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

2018 ◽  
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.

scholarly journals Robust information routing by dorsal subiculum neurons

2021 ◽  
Vol 7 (11) ◽  
pp. eabf1913
Author(s):  
Takuma Kitanishi ◽  
Ryoko Umaba ◽  
Kenji Mizuseki
Keyword(s):  
Nucleus Accumbens ◽  
Large Scale ◽  
Dorsal Hippocampus ◽  
Retrosplenial Cortex ◽  
Projection Neurons ◽  
Target Region ◽  
Ca1 Neurons ◽  
Axonal Projections ◽  
Output Structure ◽  
Hippocampal Ca1

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.

scholarly journals Hippocampal–diencephalic–cingulate networks for memory and emotion: An anatomical guide

2017 ◽  
Vol 1 ◽  
pp. 239821281772344 ◽  
Author(s):  
Emma J. Bubb ◽  
Lisa Kinnavane ◽  
John P. Aggleton
Keyword(s):  
Prefrontal Cortex ◽  
Medial Temporal Lobe ◽  
Current Knowledge ◽  
Hippocampal Formation ◽  
Retrosplenial Cortex ◽  
Thalamic Nuclei ◽  
Mammillary Bodies ◽  
Individual Site ◽  
Multi Stage ◽  
Anterior Thalamic Nuclei

This review brings together current knowledge from tract tracing studies to update and reconsider those limbic connections initially highlighted by Papez for their presumed role in emotion. These connections link hippocampal and parahippocampal regions with the mammillary bodies, the anterior thalamic nuclei, and the cingulate gyrus, all structures now strongly implicated in memory functions. An additional goal of this review is to describe the routes taken by the various connections within this network. The original descriptions of these limbic connections saw their interconnecting pathways forming a serial circuit that began and finished in the hippocampal formation. It is now clear that with the exception of the mammillary bodies, these various sites are multiply interconnected with each other, including many reciprocal connections. In addition, these same connections are topographically organised, creating further subsystems. This complex pattern of connectivity helps explain the difficulty of interpreting the functional outcome of damage to any individual site within the network. For these same reasons, Papez’s initial concept of a loop beginning and ending in the hippocampal formation needs to be seen as a much more complex system of hippocampal–diencephalic–cingulate connections. The functions of these multiple interactions might be better viewed as principally providing efferent information from the posterior medial temporal lobe. Both a subcortical diencephalic route (via the fornix) and a cortical cingulate route (via retrosplenial cortex) can be distinguished. These routes provide indirect pathways for hippocampal interactions with prefrontal cortex, with the preponderance of both sets of connections arising from the more posterior hippocampal regions. These multi-stage connections complement the direct hippocampal projections to prefrontal cortex, which principally arise from the anterior hippocampus, thereby creating longitudinal functional differences along the anterior–posterior plane of the hippocampus.

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

2019 ◽  
Vol 22 (4) ◽  
pp. 618-626 ◽  
Author(s):  
Naoki Yamawaki ◽  
Xiaojian Li ◽  
Laurie Lambot ◽  
Lynn Y. Ren ◽  
Jelena Radulovic ◽  
...  
Keyword(s):  
Long Range ◽  
Ca1 Neurons ◽  
Apical Tuft

EPS Mid-Career Award 2006: Understanding anterograde amnesia: Disconnections and hidden lesions

2008 ◽  
Vol 61 (10) ◽  
pp. 1441-1471 ◽  
Author(s):  
John P. Aggleton
Keyword(s):  
Anterograde Amnesia ◽  
Functional System ◽  
Brain Regions ◽  
Retrosplenial Cortex ◽  
Thalamic Nuclei ◽  
Neural Basis ◽  
Lesion Effect ◽  
Anterior Thalamic Nuclei ◽  
Colloid Cysts ◽  
The Many

Three emerging strands of evidence are helping to resolve the causes of the anterograde amnesia associated with damage to the diencephalon. First, new anatomical studies have refined our understanding of the links between diencephalic and temporal brain regions associated with amnesia. These studies direct attention to the limited numbers of routes linking the two regions. Second, neuropsychological studies of patients with colloid cysts confirm the importance of at least one of these routes, the fornix, for episodic memory. By combining these anatomical and neuropsychological data strong evidence emerges for the view that damage to hippocampal—mammillary body—anterior thalamic interactions is sufficient to induce amnesia. A third development is the possibility that the retrosplenial cortex provides an integrating link in this functional system. Furthermore, recent evidence indicates that the retrosplenial cortex may suffer “covert” pathology (i.e., it is functionally lesioned) following damage to the anterior thalamic nuclei or hippocampus. This shared indirect “lesion” effect on the retrosplenial cortex not only broadens our concept of the neural basis of amnesia but may also help to explain the many similarities between temporal lobe and diencephalic amnesia.

scholarly journals Anterior thalamic nuclei, but not retrosplenial cortex, lesions abolish latent inhibition in rats.

2018 ◽  
Vol 132 (5) ◽  
pp. 378-387 ◽  
Author(s):  
Andrew J. D. Nelson ◽  
Anna L. Powell ◽  
Lisa Kinnavane ◽  
John P. Aggleton
Keyword(s):  
Latent Inhibition ◽  
Retrosplenial Cortex ◽  
Thalamic Nuclei ◽  
Anterior Thalamic Nuclei

scholarly journals BIFURCATING NEURONS IN THE ANTERIOR THALAMIC NUCLEI

2021 ◽  
Author(s):  
Y Pei ◽  
S (Yee T) Tasananukorn ◽  
M Wolff ◽  
JC Dalrymple-Alford
Keyword(s):  
Hippocampal Formation ◽  
Nodal Point ◽  
Primary Source ◽  
Brain Structures ◽  
Retrosplenial Cortex ◽  
Thalamic Nuclei ◽  
Neural Ensembles ◽  
Multiple Structures ◽  
Anterior Thalamic Nuclei ◽  
New Perspective

AbstractThe anterior thalamic nuclei (ATN) form a nodal point within a hippocampal-cingulate-diencephalic memory system. ATN projections to different brain structures are conventionally viewed as distinct, but ATN neurons may send collaterals to multiple structures. The anteromedial subregion (AM) is the primary source of efferents to the medial prefrontal cortex (mPFC). Using a dual-retrograde neurotracer strategy, we discovered bifurcating AM neurons for tracers placed in the mPFC when paired with other regions. A semi-quantitative analysis found a high proportion of AM neurons (~36%) showed collateral projections when the mPFC was paired with dorsal subiculum (dSub); 20% were evident for mPFC paired with caudal retrosplenial cortex (cRSC); and 6% was found for mPFC and ventral hippocampal formation (vHF). About 10% of bifurcating AM neurons was also identified when the mPFC was not included, that is, for cRSC with dSub, and cRSC with vHF. Similar percentages of bifurcating neurons were also found within the anterior region of the adjacent nucleus reuniens (Re). The high frequency of bifurcating neurons suggests a new perspective for ATN function. These neurons would facilitate direct coordination among distal neural ensembles to support episodic memory and may explain why the ATN is a critical region for diencephalic amnesia.

scholarly journals Input to layer 1 of somatosensory cortex: Local input outweighs long-range and can modulate the activity of layer 1 interneurons

2021 ◽  
Author(s):  
Julia Ledderose ◽  
Timothy A Zolnik ◽  
Maria Toumazou ◽  
Thorsten Trimbuch ◽  
Christian Rosenmund ◽  
...  
Keyword(s):  
Somatosensory Cortex ◽  
Long Range ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Retrograde Labelling ◽  
Fast Blue ◽  
Apical Tuft ◽  
Presynaptic Boutons ◽  
A Site ◽  
Local Input

Neocortical layer (L) 1 is a locus for interactions between long-range inputs, L1 interneurons and apical tuft dendrites of pyramidal neurons. Even though we have a wealth of information about L1, the level and effect of local input to this layer have not been quantified. Here we characterized the input to L1 of mouse somatosensory cortex with fast blue, monosynaptic rabies and optogenetics. Our work shows that most of the input to L1 is local, and that both local and long-range inputs to this layer arise predominantly from L2/3 and L5 neurons. Subtypes of L5 and L6b neurons project to the overlying L1 with different probabilities. VIP and SST interneurons in L2/3 and L5 also innervate L1. A subset of local L5, the intratelencephalic, pyramidal neurons, drive L1 interneurons but have no effect on L5 apical tuft dendrites. Monosynaptic rabies-based retrograde labelling reveals presynaptic boutons covering the entire somato-dendritic axis of pyramidal neurons, including in L1. When fast blue application was combined with rabies virus, we found that only a fraction of local and long-range neurons was both presynaptic to L5 neurons and projected to L1. These results demonstrate that L1 receives a large proportion of its input from local neurons, and that some of these inputs specifically target interneurons. We conclude that L1 is not just a site for interaction between long-range feedback and apical tuft dendrites of pyramidal cells, it is also a site for complex modulation of pyramidal neurons and interneurons by local inputs.

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

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Joachim Ahlbeck ◽  
Lingzhen Song ◽  
Mattia Chini ◽  
Sebastian H Bitzenhofer ◽  
Ileana L Hanganu-Opatz
Keyword(s):  
Long Range ◽  
Pyramidal Neurons ◽  
High Efficiency ◽  
Dorsal Hippocampus ◽  
Phase Locking ◽  
Ventral Hippocampus ◽  
Neuronal Firing ◽  
Projection Neurons ◽  
Cellular Origin ◽  
Hippocampal Networks

The 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 elucidate the cellular origin of the long-range coupling in the developing brain.

scholarly journals Afferent Projections to Area Prostriata of the Mouse

2020 ◽  
Vol 14 ◽  
Author(s):  
Jin-Meng Hu ◽  
Chang-Hui Chen ◽  
Sheng-Qiang Chen ◽  
Song-Lin Ding
Keyword(s):  
Visual Information ◽  
Retrosplenial Cortex ◽  
Anterior Cingulate ◽  
Thalamic Nuclei ◽  
Unique Region ◽  
Fast Detection ◽  
Afferent Projections ◽  
Cells Of Origin ◽  
Anterior Thalamic Nuclei ◽  
Auditory Cortices

Area prostriata plays important roles in fast detection and analysis of peripheral visual information. It remains unclear whether the prostriata directly receives and integrates information from other modalities. To gain insight into this issue, we investigated brain-wide afferent projections to mouse prostriata. We find convergent projections to layer 1 of the prostriata from primary and association visual and auditory cortices; retrosplenial, lateral entorhinal, and anterior cingulate cortices; subiculum; presubiculum; and anterior thalamic nuclei. Innervation of layers 2–3 of the prostriata mainly originates from the presubiculum (including postsubiculum) and anterior midline thalamic region. Layer 5 of the prostriata mainly receives its inputs from medial entorhinal, granular retrosplenial, and medial orbitofrontal cortices and anteromedial thalamic nucleus while layer 6 gets its major inputs from ectorhinal, postrhinal, and agranular retrosplenial cortices. The claustrum, locus coeruleus, and basal forebrain provide relatively diffuse innervation to the prostriata. Moreover, Cre-dependent tracing in cortical areas reveals that the cells of origin of the prostriata inputs are located in layers 2–4 and 5 of the neocortical areas, layers 2 and 5 of the medial entorhinal cortex, and layer 5 of the retrosplenial cortex. These results indicate that the prostriata is a unique region where primary and association visual and auditory inputs directly integrate with many limbic inputs.

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