Selective information routing by ventral hippocampal CA1 projection neurons

Ciocchi, Stéphane; Passecker, Johannes; Malagon‐Vina, Hugo; Mikuš, Nace; Klausberger, Thomas

doi:10.1126/science.aaa3245

Cited by 291 publications

(395 citation statements)

References 37 publications

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“…Furthermore, the hippocampus could interact with downstream targets via multiple parallel pathways 98 , exhibiting functional dissociation during hippocampal-dependent learning between these processing streams. Interestingly, while these studies demonstrate the presence of anatomically segregated CA1PC population outputs, they also indicate the existence of CA1PCs with multiple projections 96,99 , which may coordinate the expression of inference and generalization of mnemonic processes.…”

Section: Functional Heterogeneity Of Ca1pc In the Context Of Behaviormentioning

confidence: 92%

“…Recent studies have provided compelling evidence for such selective routing of information to downstream targets via projection-specific CAPC subpopulations. For example, anxiety-related, goal-directed, and SPWR-related firing are selectively increased in CA1PCs projecting to the prefrontal cortex, nucleus accumbens, and in triple-projecting neurons (targeting the prefrontal cortex, amygdala, and nucleus accumbens), respectively 96 . Further, CA1PCs projecting to the nucleus accumbens shell from the ventral hippocampus, preferentially located in the deep sublayer, play a necessary and sufficient role in social memory 97 .…”

Section: Functional Heterogeneity Of Ca1pc In the Context Of Behaviormentioning

confidence: 99%

“…The functional segregation of CA1PCs along the superficial–deep, dorsoventral and proximodistal axes, accompanied by spatial differences in gene expression (Box 2) and specific behavioral roles of target-specific CA1PC subpopulations 46,47,96–98 , implies the existence of a multiplicity of parallel, nonuniform hippocampal subcircuits. However, an even larger and finer-grained array of segregated parallel subcircuits may exist in relation to timing of embryonic neurogenesis, as indicated by evidence that CA3 pyramidal cells (CA3PCs) form selective interconnections with their birthdate-related partners in the CA1 100,101 .…”

Section: Open Questions About Heterogeneity Of Principal Neurons In Tmentioning

confidence: 99%

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CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus

2018

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Hippocampal network operations supporting spatial navigation and declarative memory are traditionally interpreted in a framework where each hippocampal area, such as the dentate gyrus, CA3, and CA1, consists of homogeneous populations of functionally equivalent principal neurons. However, heterogeneity within hippocampal principal cell populations, in particular within pyramidal cells at the main CA1 output node, is increasingly recognized and includes developmental, molecular, anatomical, and functional differences. Here we review recent progress in the delineation of hippocampal principal cell subpopulations by focusing on radially defined subpopulations of CA1 pyramidal cells, and we consider how functional segregation of information streams, in parallel channels with nonuniform properties, could represent a general organizational principle of the hippocampus supporting diverse behaviors.

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Section: Functional Heterogeneity Of Ca1pc In the Context Of Behaviormentioning

confidence: 92%

Section: Functional Heterogeneity Of Ca1pc In the Context Of Behaviormentioning

confidence: 99%

Section: Open Questions About Heterogeneity Of Principal Neurons In Tmentioning

confidence: 99%

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CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus

2018

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“…The hippocampus is the main focus of this study not only due to it being distinctly vulnerable to traumatic and excitotoxic injuries, but also because it is a region that is important for higher order brain functions, that expresses synaptic plasticity to compute diverse information, and that is involved in routing encoded spatial, emotional, and reward information to other brain areas (see Bahr et al, 1998; Szinyei et al, 1999; Pelletier and Lacaille, 2008; Schober et al, 2014; Carlson et al, 2015; Ciocchi et al, 2015). The organotypic cultures allow studies to address specific issues in the absence of systemic variables, thus avoiding interpretation issues in the present study regarding whether subtle vs. severe neuronal changes are produced by single or multiple RDX blasts.…”

Section: Introductionmentioning

confidence: 99%

Blast waves from detonated military explosive reduce GluR1 and synaptophysin levels in hippocampal slice cultures

Smith

Piehler

Benjamin

et al. 2016

Experimental Neurology

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Explosives create shockwaves that cause blast-induced neurotrauma, one of the most common types of traumatic brain injury (TBI) linked to military service. Blast-induced TBIs are often associated with reduced cognitive and behavioral functions due to a variety of factors. To study the direct effects of military explosive blasts on brain tissue, we removed systemic factors by utilizing rat hippocampal slice cultures. The long-term slice cultures were briefly sealed air-tight in serum-free medium, lowered into a 37 °C water-filled tank, and small 1.7-gram assemblies of cyclotrimethylene trinitramine (RDX) were detonated 15 cm outside the tank, creating a distinct shockwave recorded at the culture plate position. Compared to control mock-treated groups of slices that received equal submerge time, 1–3 blast impacts caused a dose-dependent reduction in the AMPA receptor subunit GluR1. While only a small reduction was found in hippocampal slices exposed to a single RDX blast and harvested 1–2 days later, slices that received two consecutive RDX blasts 4 min apart exhibited a 26–40% reduction in GluR1, and the receptor subunit was further reduced by 64–72% after three consecutive blasts. Such loss correlated with increased levels of HDAC2, a histone deacetylase implicated in stress-induced reduction of glutamatergic transmission. No evidence of synaptic marker recovery was found at 72 h post-blast. The presynaptic marker synaptophysin was found to have similar susceptibility as GluR1 to the multiple explosive detonations. In contrast to the synaptic protein reductions, actin levels were unchanged, spectrin breakdown was not detected, and Fluoro-Jade B staining found no indication of degenerating neurons in slices exposed to three RDX blasts, suggesting that small, sub-lethal explosives are capable of producing selective alterations to synaptic integrity. Together, these results indicate that blast waves from military explosive cause signs of synaptic compromise without producing severe neurodegeneration, perhaps explaining the cognitive and behavioral changes in those blast-induced TBI sufferers that have no detectable neuropathology.

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“…Interestingly, using a combined approach of optogenetics and electrophysiology, Ciocchi et al (2015) demonstrated that the ventral hippocampus is capable of sending information of emotional content to specific neurone populations in the amygdala, nucleus accumbens and medial prefrontal cortex. In a combined experimental approach of multi-site neural recording and optogenetics, Padilla-Coreano et al (2016) showed that inhibition of ventral hippocampus input to the medial prefrontal cortex disrupts the behavioural expression of anxiety.…”

Section: Structural and Functional Segregation Of The Hippocampusmentioning

confidence: 99%

Limbic modulation of the autonomic nervous system

Ajayi¹

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Nuclei in the hypothalamus and brainstem are responsible for maintaining homoeostasis by controlling rhythmic motor and autonomic activities. However, during emotional responses to real or potential environmental challenges, significant changes in motor and autonomic rhythm also occur.Forebrain structures that form the limbic system are responsible for perceiving environmental challenges and orchestrating appropriate emotional responses. Thus, it is only through descending synaptic interactions of the forebrain areas with the hypothalamus and brainstem, that modulation of motor and autonomic activities is possible during the expression of emotions. However, there is little knowledge of the forebrain areas that modulate autonomic activities. Also, in coordinating physiologic responses, forebrain structures operate through functional networks but the neural pathways and mechanisms involved particularly during emotional behaviours are not clear.The hippocampus is an important component of the limbic system involved in learning and memory, but evolving evidence implicates it in the expression of emotions such as defensive fear and anxiety reactions. Studies also suggest possible hippocampal connections with brainstem autonomic centres.Thus, the central hypothesis tested in this thesis is that discrete neurone populations in the ventral hippocampus, via neuronal projections to the amygdala, can modulate bulbar motor and autonomic output. Specific aims were to 1) Investigate and describe the respiratory and cardiovascular changes induced by chemically mapping the dorsal and ventral hippocampus with microinjections of the excitatory amino acid, D, L-Homocysteic acid, 2) Investigate the distribution of descending projections of the hippocampus using classical neuroanatomical tract tracing techniques, with a particular focus on the connectivity of the ventral hippocampus and the amygdala, 3) To extend the chemical mapping to specific areas in the amygdala that receive projections from the hippocampus and determine how such areas differ in their influence over motor and autonomic functions and 4) To investigate the effects of inhibiting of the amygdala while stimulating the ventral hippocampus.Experiments were conducted using urethane-anaesthetised (1.5 g/kg IP) adult Sprague-Dawley rats (n = 136; weight = 300 -600 g; either sex). The hippocampus was stereotaxically mapped to locate discrete neurone populations that can modulate motor and autonomic activities. The specific parameters monitored include blood pressure, heart rate, respiratory frequency, inspiratory and expiratory durations, tracheal pressure and the motor expression of augmented breaths.Microinjections of the excitatory amino acid (EAA), D, L, Homocysteic acid (DLH; 50 mM, pH 7.4, iii n = 95), were used for chemical stimulation. Using this stimulation technique, discrete neurone populations in the ventral hippocampus were identified that can generate significant changes in both respiratory and cardiovascular parameters. Augmented breaths, which have...

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Selective information routing by ventral hippocampal CA1 projection neurons

Cited by 291 publications

References 37 publications

CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus

CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus

Blast waves from detonated military explosive reduce GluR1 and synaptophysin levels in hippocampal slice cultures

Limbic modulation of the autonomic nervous system

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