Robust information routing by dorsal subiculum neurons

The dorsal hippocampus conveys various information associated with spatial navigation; however, how the information is distributed to multiple downstream areas remains unknown. We investigated this by identifying axonal projections using optogenetics during large-scale recordings from the rat subiculum, the major hippocampal output structure. Subicular neurons demonstrated a noise-resistant representation of place, speed, and trajectory, which was as accurate as or even more accurate than that of hippocampal CA1 neurons. Speed- and trajectory-dependent firings were most prominent in neurons projecting to the retrosplenial cortex and nucleus accumbens, respectively. Place-related firing was uniformly observed in neurons targeting the retrosplenial cortex, nucleus accumbens, anteroventral thalamus, and medial mammillary body. Theta oscillations and sharp-wave/ripples tightly controlled the firing of projection neurons in a target region–specific manner. In conclusion, the dorsal subiculum robustly routes diverse navigation-associated information to downstream areas.

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Robust information routing by dorsal subiculum neurons

10.1101/2020.06.04.133256 ◽

2020 ◽

Author(s):

Takuma Kitanishi ◽

Ryoko Umaba ◽

Kenji Mizuseki

Keyword(s):

Nucleus Accumbens ◽

Large Scale ◽

Retrosplenial Cortex ◽

Projection Neurons ◽

Target Region ◽

Ca1 Neurons ◽

Axonal Projections ◽

Output Structure ◽

Hippocampal Ca1 ◽

Specific Manner

AbstractThe hippocampus conveys various information associated with spatial navigation; yet, information distribution to multiple downstream areas remains unknown. We investigated this by identifying axonal projections using optogenetics during large-scale recordings from the rat subiculum, the major hippocampal output structure. Subicular neurons demonstrated a noise-resistant representation of place, speed, and trajectory, which was as accurate as that of hippocampal CA1 neurons. Speed and trajectory information was most prominently sent to the retrosplenial cortex and nucleus accumbens, respectively. Place information was distributed uniformly to the retrosplenial cortex, nucleus accumbens, anteroventral thalamus, and medial mammillary body. Information transmission by projection neurons was tightly controlled by theta oscillations and sharp-wave/ripples in a target region-specific manner. In conclusion, the subiculum robustly routes diverse navigation-associated information to downstream areas.One Sentence SummaryThe subiculum accurately and robustly represents diverse information and routes it in a target region-specific manner.

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Long-range inhibitory intersection of a retrosplenial thalamocortical circuit by apical tuft-targeting CA1 neurons

10.1101/427179 ◽

2018 ◽

Cited By ~ 3

Author(s):

Naoki Yamawaki ◽

Xiaojian Li ◽

Laurie Lambot ◽

Lynn Y. Ren ◽

Jelena Radulovic ◽

...

Keyword(s):

Long Range ◽

Pyramidal Neurons ◽

Dorsal Hippocampus ◽

Retrosplenial Cortex ◽

Molecular Profile ◽

Thalamic Nuclei ◽

Cellular Mechanisms ◽

Ca1 Neurons ◽

Apical Tuft ◽

Anterior Thalamic Nuclei

AbstractDorsal hippocampus, retrosplenial cortex (RSC), and anterior thalamic nuclei (ATN) interact to mediate diverse cognitive functions, but the cellular basis for these interactions is unclear. We hypothesized a long-range circuit converging in layer 1 (L1) of RSC, based on the pathway anatomy of GABAergic CA1 retrosplenial-projecting (CA1-RP) neurons and thalamo-restrosplenial projections from ATN. We find that CA1→RSC projections stem from GABAergic neurons with a distinct morphology, electrophysiology, and molecular profile, likely corresponding to recently described Ntng1-expressing hippocampal interneurons. CA1-RP neurons monosynaptically inhibit L5 pyramidal neurons, principal outputs of RSC, via potent GABAergic synapses onto apical tuft dendrites in L1. These inhibitory inputs align precisely with L1-targeting thalamocortical excitatory inputs from ATN, particularly the anteroventral nucleus, forming a convergent circuit whereby CA1 inhibition can intercept ATN excitation to co-regulate RSC activity. Excitatory axons from subiculum, in contrast, innervate proximal dendrites in deeper layers. Short-term synaptic plasticity differs at each connection. Chemogenetically abrogating inhibitory CA1→RSC or excitatory ATN→RSC connections oppositely affects the encoding of contextual fear memory. Collectively, our findings identify multiple cellular mechanisms underlying hippocampo-thalamo-retrosplenial interactions, establishing CA1 RSC-projecting neurons as a distinct class with long-range axons that target apical tuft dendrites, and delineating an unusual cortical circuit in the RSC specialized for integrating long-range inhibition and thalamocortical excitation.

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Glutamatergic drive along the septo-temporal axis of hippocampus boosts prelimbic oscillations in the neonatal mouse

10.1101/222166 ◽

2017 ◽

Cited By ~ 1

Author(s):

Joachim Ahlbeck ◽

Lingzhen Song ◽

Mattia Chini ◽

Antonio Candela ◽

Sebastian H. Bitzenhofer ◽

...

Keyword(s):

Long Range ◽

Hippocampal Neurons ◽

High Efficiency ◽

Dorsal Hippocampus ◽

Phase Locking ◽

Ventral Hippocampus ◽

Neuronal Firing ◽

Projection Neurons ◽

List Type ◽

Axonal Projections

SUMMARYThe long-range coupling within prefrontal-hippocampal networks that account for cognitive performance emerges early in life. The discontinuous hippocampal theta bursts have been proposed to drive the generation of neonatal prefrontal oscillations, yet the cellular substrate of these early interactions is still unresolved. Here, we selectively target optogenetic manipulation of glutamatergic projection neurons in the CA1 area of either dorsal or intermediate/ventral hippocampus at neonatal age to elucidate their contribution to the emergence of prefrontal oscillatory entrainment. We show that despite stronger theta and ripples power in dorsal hippocampus, the prefrontal cortex is mainly coupled with intermediate/ventral hippocampus by phase-locking of neuronal firing via dense direct axonal projections. Theta band-confined activation by light of pyramidal neurons in intermediate/ventral but not dorsal CA1 that were transfected by in utero electroporation with high-efficiency channelrhodopsin boosts prefrontal oscillations. Our data causally elucidates the cellular origin of the long-range coupling in the developing brain.HighlightsNeonatal theta bursts, sharp waves and ripples vary along septo-temporal axisHippocampal activity times prefrontal oscillations via direct axonal projectionsSelective hippocampal targeting along septo-temporal axis causes precise firingLight stimulation of hippocampal neurons at 8 Hz boosts prefrontal oscillations

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Watermaze Learning Enhances Excitability of CA1 Pyramidal Neurons

Journal of Neurophysiology ◽

10.1152/jn.01177.2002 ◽

2003 ◽

Vol 90 (4) ◽

pp. 2171-2179 ◽

Cited By ~ 103

Author(s):

M. Matthew Oh ◽

Amy G. Kuo ◽

Wendy W. Wu ◽

Evgeny A. Sametsky ◽

John F. Disterhoft

Keyword(s):

Pyramidal Neurons ◽

Dorsal Hippocampus ◽

Eyeblink Conditioning ◽

Hippocampal Pyramidal Neurons ◽

Ca1 Neurons ◽

Ca1 Pyramidal Neurons ◽

Platform Location ◽

Dorsal Hippocampal ◽

Hippocampal Ca1 ◽

Trace Eyeblink Conditioning

The dorsal hippocampus is crucial for learning the hidden-platform location in the hippocampus-dependent, spatial watermaze task. We have previously demonstrated that the postburst afterhyperpolarization (AHP) of hippocampal pyramidal neurons is reduced after acquisition of the hippocampus-dependent, temporal trace eyeblink conditioning task. We report here that the AHP and one or more of its associated currents ( IAHP and/or s IAHP) are reduced in dorsal hippocampal CA1 pyramidal neurons from rats that learned the watermaze task as compared with neurons from control rats. This reduction was a learning-induced phenomenon as the AHP of CA1 neurons from rats that failed to learn the hidden-platform location was similar to that of neurons from control rats. We propose that reduction of the AHP in pyramidal neurons in regions crucial for learning is a cellular mechanism of learning that is conserved across species and tasks.

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