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Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop
Open accessAbstract
Neurons propagate information through circuits by integrating thousands of synaptic inputs to generate an action potential output. Inputs from different origins are often targeted to distinct regions of a neuron’s dendritic tree, with synapses on more distal dendrites normally having a weaker influence on cellular output compared to synapses on more proximal dendrites. Here we report that hippocampal CA2 pyramidal neurons, whose function has remained obscure for 75 years, have a reversed synaptic strength rule. Thus, CA2 neurons are strongly excited by their distal dendritic inputs from entorhinal cortex but only weakly activated by their more proximal dendritic inputs from hippocampal CA3 neurons. CA2 neurons in turn make strong excitatory synaptic contacts with CA1 neurons. In this manner CA2 neurons form the nexus of a highly plastic disynaptic circuit linking the cortical input to the hippocampus to its CA1 neuronal ouput. This circuit is likely to mediate key aspects of hippocampal-dependent spatial memory.
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TL;DR
This paper shows that hippocampal CA2 pyramidal neurons obey a reversed synaptic-strength rule: distal entorhinal cortical inputs strongly excite them, while proximal CA3 inputs are weak and inhibition-dominated. CA2 neurons in turn form unusually strong excitatory connections onto CA1 neurons, defining a plastic disynaptic cortico-hippocampal loop.
Key findings
- Distal entorhinal inputs drive CA2 far more strongly than CA1: LIII stimulation (20 V) evoked EPSPs of 9.4 ± 1.2 mV in CA2 versus 1.9 ± 0.4 mV in CA1 (n = 10 vs 8, p < 0.001); LII stimulation (20 V) evoked 7.4 ± 0.9 mV in CA2 versus 2.8 ± 0.8 mV in CA3 (n = 8 vs 6, p < 0.003).
- Proximal CA3/Schaffer collateral inputs are weaker onto CA2 and dominated by feed-forward inhibition: SC EPSPs were 10.8 ± 2.2 mV in CA2 versus 17.5 ± 2.6 mV in CA1 (n = 7 vs 8, p = 0.008), with similar IPSPs, giving EPSP/IPSP < 1 in CA2 versus ~2 in CA1. With inhibition intact, LIII stimulation fired CA2 in 20% of cells (3/15) but not CA1; with inhibition blocked, LIII fired 80% of CA2 neurons (12/15) but only 1/12 CA1 neurons.
- Cortical synapses onto CA2 express robust LTP: LIII–CA2 fEPSPs potentiated to 162.5 ± 9.1% (n = 9) versus 127.1 ± 5.4% at LIII–CA1 (n = 7, p = 0.01); LII–CA2 LTP was 194.3 ± 9.8% (n = 6) versus 135.1 ± 9.3% at LII–CA3 (n = 6, p = 0.0008). SC–CA2 LTP was weak/transient (108.9 ± 4.2%, n = 9) versus CA1 (153.5 ± 13.0%, n = 9, p = 0.006).
- CA2–CA1 unitary connections are strong: connectivity was ~5% (5 out of ~100 pairs tested), success probability 0.4–0.6, and potency ~−8 pA versus ~−4 pA reported for CA3–CA1; EPSC successes showed multiple equally spaced peaks around −5 pA. LIII stimulation could drive CA2 firing and then a late polysynaptic CA1 response/action potential; cutting between CA2 and CA1 abolished this (n = 8), while cutting between CA3 and CA2 preserved it in 4/6 experiments.
Methods
- Acute transverse hippocampal slices from 4–6 week old C57BL6 male mice; whole-cell current-clamp recordings from CA1, CA2, and CA3 pyramidal neurons, extracellular field recordings, and paired CA2–CA1 recordings.
- Synaptic inputs were activated by focal stimulation in stratum lacunosum moleculare (LIII EC), dentate molecular layer (LII EC), and stratum radiatum (Schaffer collaterals); inhibitory transmission was blocked with picrotoxin and CGP 55845A, and polysynaptic DG→CA3→CA2 responses were blocked with DCG-IV.
- CA2 identity was confirmed by electrophysiological criteria, morphology, fluorescent dye filling, and post hoc α-actinin 2 immunolabeling. LTP was induced by tetanic stimulation (100 pulses at 100 Hz, repeated twice at 20 s intervals) and measured 40–50 min after induction versus baseline; comparisons used Student’s t-test, reported as mean ± SEM.
Limitations
- Stated: paired CA2–CA1 connectivity was very low (~5%, 5 out of ~100 pairs tested), limiting detailed characterization; only three of five connected pairs were studied with dual whole-cell recordings and two with extracellular stimulation of a single CA2 neuron.
- Stated: additional studies are needed to elucidate the dendritic mechanisms underlying differential EPSP propagation in CA2 versus CA1, and future chemical or genetic lesions of CA2 are needed to define its role in the intact hippocampus.
- Evident: all experiments are in acute hippocampal slices from young adult male mice, so circuit function, memory roles, and in vivo firing inferences are not directly tested here; the authors address some slice-artifact concerns with field recordings and comparisons to prior in vivo work, but the study remains in vitro.
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59 Own result · 27 Own interpretation · 23 Not checked yet · 6 Own method · 6 No basis given
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In the paper
“Surprisingly, the same stimulation had a much stronger impact on CA2 pyramidal neurons, generating somatic EPSPs up to 5 times larger than those in CA1 (Fig. 2A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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“This is in contrast with the morphology of CA1 neurons, which have a main apical dendrite that either did not bifurcate within SR or bifurcated far from the soma (107.6 ± 11.1 μm, n = 14).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
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In the paper
“Finally, the depolarizing sag in response to a hyperpolarizing current pulse, which is caused by the hyperpolarization-activated cation current (Ih), was much larger in CA1 neurons than in CA2 neurons (Fig. 1B and Table 1).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
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“In contrast, CA3 inputs onto proximal CA2 neuron dendrites are relatively weak, dominated by feed-forward inhibition, and fail to undergo LTP.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > INTRODUCTION
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“As previously reported (Empson and Heinemann, 1995b), focal stimulation of the LIII EC axons (perforant path) in SLM elicited only very small EPSPs in the CA1 neuron soma, even with inhibitory transmission blocked by GABAA and GABAB receptor antagonists (Fig. 2A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
What the sources say
- Not checked yetcites Empson and Heinemann, 1995b
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In the paper
“In contrast, CA3 inputs onto proximal CA2 neuron dendrites are relatively weak, dominated by feed-forward inhibition, and fail to undergo LTP.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > INTRODUCTION
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“CA2 neurons were further distinguished from CA1 neurons because the prominent slow after-hyperpolarization present in CA1 neurons was absent in CA2 neurons (Fig. 1A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
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“Finally, CA2 neurons make unusually strong unitary connections with CA1 neurons, forming a potent disynaptic circuit, independent of the trisynaptic path, that is powerfully regulated by long-term synaptic plasticity.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > INTRODUCTION
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“In addition, CA2 neurons had a much larger soma than CA1 neurons (surface area of 391 ± 22 μm2 in CA2 versus 179 ± 11 μm2 in CA1).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
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“Thus, the IPSP (elicited by a 20 V stimulus) was −2.3 ± 0.4 mV in CA1 (n = 8) versus −3.7 ± 1.2 mV in CA2 (n = 8; p = 0.26; Fig. 2C).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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“In contrast, CA3 inputs onto proximal CA2 neuron dendrites are relatively weak, dominated by feed-forward inhibition, and fail to undergo LTP.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > INTRODUCTION
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“Thus a moderately strong 20 V extracellular stimulus elicited a mean EPSP of only 1.9 ± 0.4 mV (n = 8) in CA1 neurons versus an EPSP of 9.4 ± 1.2 mV (n = 10) in CA2 neurons ( p<0.001).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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“Thus the SC EPSP (elicited by a 16 V stimulus) was equal to 17.5 ± 2.6 mV in CA1 (n = 8) versus 10.8 ± 2.2 mV in CA2 (n = 7; p = 0.008, Fig. 3A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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“We obtained similar results using extracellular field recordings of the population spike (PS) in the CA1 and CA2 somatic layers: single or paired stimulation of LIII inputs consistently evoked a PS in CA2 but not in CA1, where only a small field EPSP was present.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
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“A 20 V stimulus intensity elicited an EPSP of 2.8 ± 0.8 mV in CA3 neurons (n = 6) versus 7.4 ± 0.9 mV in CA2 (n = 8; p<0.003; Fig. 5B).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
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“In contrast, LIII stimulation produced a net depolarization in CA2 neurons that was sufficient to trigger one or more spikes in 20% of cells tested (n = 3/15, Fig. 4A,B).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
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“Thus, activation of SC inputs (by a 16 V stimulus in SR) elicited an IPSP of −12.6 ± 2.9 mV in CA1 (n = 8) versus an IPSP of −13.8 ± 2.4 mV in CA2 (n = 7; p > 0.5).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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“As expected, the SCs exerted a powerful excitatory drive in CA1, triggering spikes in over 1/3 of neurons tested (n = 4/11, Fig. 4D,E).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
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“In contrast, the small size of the EPSPs in CA1 neurons resulted in an EPSP/IPSP ratio close to (or slightly less than) one.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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“In contrast to the lack of LTP at CA3–CA2 synapses, we observed a surprisingly large and robust LTP of LIII CA2 fEPSPs (162.5 ± 9.1%, n = 9).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
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“As reported for CA3–CA1 connections (Bolshakov and Siegelbaum, 1995), the probability of connectivity between CA2 and CA1 neurons was very low in transverse slices (~5%, 5 out of ~100 pairs tested), limiting our ability to obtain detailed data.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
What the sources say
- Not checked yetcites Bolshakov and Siegelbaum, 1995
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“As expected for quantal synaptic transmission, successive presynaptic stimuli either elicited unitary EPSCs of variable amplitude (successes) or failed to trigger an EPSC (failures).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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- Rests on an assumption: Synaptic transmission at CA2–CA1 synapses is quantal.
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In the paper
“Local stimulation of fibers in either the SR or SO regions of CA1 routinely was able to elicit antidromic spikes in the somatic layer of CA2.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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“However, our results confirmed the previous whole-cell findings as high-frequency tetanic stimulation (HFS) of the SC inputs led to only a small and transient potentiation of the CA2 fEPSPs (Fig. 7A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
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“In contrast, and as expected, a large LTP was observed for the SC fEPSPs in CA1 neurons (Fig. 7A. 153.5 ± 13.0% [n = 9] in CA1; 108.9 ± 4.2 % [n = 9] in CA2; p = 0.006).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
plainn = 9- Asserted: passes — The authors put it forward as true.
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“Indeed, all CA2 neurons exhibited EPSPs in response to independent stimulation of both LII and LIII inputs (n = 20).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
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“Upon focal stimulation in either SLM of CA1 or the molecular layer of DG, the largest field potential response was observed in the CA2 cell body area (Fig. 5C).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
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“Moreover, this LTP was also much greater than the weak LTP observed at the LIII inputs to CA1 (127.1 ± 5.4%, n = 7; p = 0.01; Fig. 7B).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
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“In contrast, an antidromic spike was only elicited in CA3 neurons when the stimulating electrode was placed in SR, but not in SO, of CA1.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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“However, polysynaptic responses and action potentials were never evoked in CA1 neurons when slices were cut between CA2 and CA1, even with stronger LIII stimulation (up to 60 V, n = 8, Fig. 9B).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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“However, when we increased the stimulus strength to 20–40 V, a large, late polysynaptic EPSP was elicited in the CA1 neurons that eventually reached threshold for firing an action potential (Fig. 9A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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“However, the potency (average amplitude of EPSC successes) was about two-fold larger at CA2–CA1 synapses, around −8 pA (Fig. 8D), than previously reported for CA3–CA1 synapses, around−4 pA (see (Bolshakov and Siegelbaum, 1995; McMahon et al., 1996).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
What the sources say
- Not checked yetcites Bolshakov and Siegelbaum, 1995
- Not checked yetcites McMahon et al., 1996 source
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- Rests on an assumption: Synaptic transmission at CA2–CA1 synapses is quantal.
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In the paper
“Furthermore, the polysynaptic response in CA1 was present when slices were cut between CA3 and CA2 in 4/6 experiments, indicating that CA3 was not involved in this process.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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In the paper
“In addition to the unexpectedly large excitatory drive that the distal EC inputs exert on CA2 neurons, we find that the SC inputs from CA3 neurons recruit a very large feedforward inhibition onto the CA2 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
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In the paper
“In one pair of CA2 and CA1 neurons, we observed five distinct peaks of equally spaced EPSC successes (Fig. 8C).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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- Rests on an assumption: Synaptic transmission at CA2–CA1 synapses is quantal.
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In the paper
“As described above, moderate intensity stimulation of LIII axons ( 15 V) evoked only a small, direct EPSP in the CA1 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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In the paper
“This polysynaptic response was only observed when the LIII stimulation elicited spikes in CA2 neurons, as indicated by simultaneous extracellular recordings of the PS in the CA2 somatic layer (Fig. 9A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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In the paper
“In contrast, CA2 neurons display a reversed pattern of synaptic strength, with the distal EC inputs providing a much larger excitatory drive compared to the proximal SC inputs.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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In the paper
“Moreover, based on the size of the depolarizing sag in response to a hyperpolarizing current pulse, there is also a much lower density of Ih in the CA2 somato-dendritic compartment compared to CA1 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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In the paper
“However, the presence of sublinear summation between layer II and layer III EPSPs argues against this possibility.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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In the paper
“First, the somatic EPSPs elicited by distal (EC) stimulation are five-fold larger in CA2 versus CA1 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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In the paper
“Thus, we found that the distal synaptic current density (measured by the fEPSP) in response to distal stimulation in SLM is identical in CA1 and CA2.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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In the paper
“This normal pattern of synaptic drive is apparent in CA1 pyramidal neurons, where activation of the distal synaptic inputs from EC produces a much smaller somatic EPSP compared to activation of the more proximal SC inputs.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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In the paper
“Second, the somatic EPSPs elicited by proximal (SC) stimulation are smaller in CA2 than CA1 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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In the paper
“This circuit is likely to mediate key aspects of hippocampal-dependent spatial memory.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > Abstract
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In the paper
“One potential concern with such results is that the difference in excitatory drive is an artifact caused by differences in the extent to which the EC inputs to the CA1 and CA2 regions are preserved in the hippocampal slice preparation or activated by the focal stimulating electrode. However, three lines of evidence argue that the difference is genuine.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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In the paper
“This difference is consistent with the higher levels of expression of the HCN1 subunit, which underlies Ih, in CA1 neurons compared to CA2 or CA3 neurons (Notomi and Shigemoto, 2004; Santoro et al., 2004).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
What the sources say
- Not checked yetcites Notomi and Shigemoto, 2004
- Not checked yetcites Santoro et al., 2004 source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Altogether, these data show that CA1 and CA2 pyramidal neurons display a reversed net synaptic drive along their apical dendrites in response to stimulation of their EC versus SC inputs that is caused by differences in the strength of the underlying EPSPs.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
boosteddirectn = 8- Asserted: passes — The authors put it forward as true.
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In the paper
“These field recording results indicate that the differential ability of LIII inputs to drive firing in CA2 but not CA1 is genuine and not an artifact of the whole-cell recordings.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
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In the paper
“This likely resulted from saturation as the distal EPSPs approached their reversal potential, and not from recruitment of an inhibitory component, as similar results were observed with inhibition blocked (data not shown).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
hedgedconditionaln = 20- Asserted: passes — The authors put it forward as true.
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In the paper
“These results are consistent with the known anatomical innervation patterns of CA2 and CA3 axons and confirm that CA2 axons do indeed project to both SR and SO of CA1 (Fig. 8A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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In the paper
“In contrast, CA2 neurons are largely inhibited by their intra-hippocampal input from CA3 pyramidal neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION
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In the paper
“Because this strong inhibition is initially engaged by the same input that directly activates CA2 (layer II input), it will preserve independence between the di- and the triynaptic loops.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
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In the paper
“The good agreement between these in vivo recordings and our findings indicates that the differential synaptic responses we observe among CA1, CA2 and CA3 neurons are genuine and not an artifact of the hippocampal slice preparation.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION
What the sources say
- Not checked yetcites Bartesaghi and Gessi, 2004
- Not checked yetcites Bartesaghi et al., 2006 source
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In the paper
“Second, CA2 neurons strongly excite CA1 pyramidal neurons through potent excitatory synaptic connections.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“indicating that CA3 was not involved in this process.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“Fourth, the inputs to CA2 neurons from CA3 neurons recruit strong feed-forward inhibition.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“The weak excitatory drive of the cortical inputs to CA1 neurons likely restricts these inputs to a modulatory role in regulating CA1 output, for example, providing instructive signals for the induction of plasticity at the more potent CA3 inputs (Dudman et al., 2007; Judge and Hasselmo, 2004; Levy et al., 1998; Remondes and Schuman, 2002).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
What the sources say
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“The difference in size of somatic EPSPs in CA1 versus CA2 neurons elicited by distal EC stimulation is likely to reflect intrinsic differences in the extent to which the distal dendrites of the two neurons integrate and attenuate the local EPSP as it propagates to the soma, rather than to differences in the efficacy of local synaptic transmission.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
hedgedconditional- Asserted: passes — The authors put it forward as true.
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- Rests on an assumption: Excitatory synaptic inputs terminating on distal dendrites usually provide weaker somatic drive than proximal inputs due to cable properties.
None of the sources cited for this claim have been checked yet.
In the paper
“In contrast, immunocytochemical light micrographs show that HCN1 channels fail to accumulate in the distal CA2 dendrites (Notomi and Shigemoto, 2004; Santoro et al., 2004).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
What the sources say
- Not checked yetcites Notomi and Shigemoto, 2004
- Not checked yetcites Santoro et al., 2004 source
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Our findings also demonstrate how the synaptic drive of the same class of LIII EC inputs onto neighboring CA1 and CA2 neurons can be tuned to differentially route information through the hippocampal circuit.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Second, distal EPSPs in CA1 neurons are locally attenuated by the active properties of the dendrites, including the presence of a very high density of HCN1 channels in the distal dendrites, which act as a depolarizing shunt conductance (George et al., 2009; Magee, 1999).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
What the sources say
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“the CA2 dendritic cable can produce at most a 7-fold attenuation of the distal EPSP”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
plaindirect- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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- Rests on an assumption: Excitatory synaptic inputs terminating on distal dendrites usually provide weaker somatic drive than proximal inputs due to cable properties.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This suggests that CA2 neurons may play an important role in the modulation and synchronization of activity throughout the hippocampal network.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“Thus, mice lacking the vasopressin V1b receptor, which is highly expressed in CA2 neurons (Young et al., 2006), show a selective impairment in episodic memory of the temporal order of events (DeVito et al., 2009).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
What the sources say
plaindirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“the distal EC inputs are likely to provide a strong excitatory drive to the CA2 neurons in awake animals, given the fact that the SC inputs to CA2 neurons recruit a large net feedforward inhibition.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“In addition, lesions at the CA3/CA2 border impair hippocampal-dependent operant conditioning (Samuel et al., 1997).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
What the sources say
- Not checked yetcites Samuel et al., 1997 source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“The cortico-CA2 synapses are also likely to contribute to hippocampal function and memory formation under normal conditions when CA3 inputs are intact.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“Moreover, the finding that CA2 neurons exhibit place cell firing in vivo similar to CA1 neurons (Martig and Mizumori, 2010) indicates that the distal EC inputs are likely to provide a strong excitatory drive to the CA2 neurons in awake animals, given the fact that the SC inputs to CA2 neurons recruit a large net feedforward inhibition.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
What the sources say
- Not checked yetcites Martig and Mizumori, 2010
plaincorrelational- Asserted: passes — The authors put it forward as true.
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- It may state two separate claims as one. 51
- Probably not a substantial claim. 4
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, the CA2 neuron input resistance was lower and the membrane capacitance was higher compared to CA1 or CA3 neurons (see Table 1).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Although LIII stimulation still evoked a large net depolarizing response in CA2 neurons, there was now often a net hyperpolarizing response observed in CA1 neurons (Fig. 2C).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
hedgeddirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, the apical dendrite bifurcated close to the soma (31.1 ± 3.6μm, n = 19) into two or three main branches that extended to stratum lacunosum moleculare (SLM) with few secondary, oblique branches in stratum radiatum (SR) but many branches in SLM (Fig. 1C and. Fig. S1).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
plainn = 19- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, the large CA2 EPSPs ensured the presence of a net depolarizing response even when inhibition was intact, with a 3–4 fold ratio of excitation to inhibition (Fig. 2D).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
plaindirectn = 8- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The hyperpolarization in CA1 was not due to a lack of excitatory inputs as all CA1 neurons exhibited a clear EPSP in response to LIII stimulation in the presence of GABA blockers (n=24 out of 24 neurons).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
boostedn = 24- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Moreover, whereas CA3 neurons fired a burst of action potentials at the beginning of a depolarizing current step, CA1 and CA2 neurons fired during the entire depolarization (Fig. 1A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Stronger stimulation of LII inputs evoked a large inhibitory response, and addition of GABA blockers unmasked polysynaptic EPSPs (Fig. 5A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
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In the paper
“Activation of LII inputs with a moderate stimulus produced surprisingly large EPSPs in CA2 neurons with little synaptic delay, indicating they were monosynaptic responses.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
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In the paper
“In contrast, SC stimulation never led to firing in CA2 (n = 0/8) but rather elicited a large net hyperpolarizing response (Fig. 4D,E).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
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In the paper
“Blocking inhibition greatly increased the efficiency of spike firing in CA1 neurons, with 100% of neurons firing spikes (11/11), and also enabled the SC inputs to trigger spikes in the majority of CA2 neurons (75%, n = 6/8, Fig. 4F).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
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In the paper
“As a result, SC stimulation produced a large net depolarization in CA1 neurons (EPSP/IPSP ratio ~2), whereas inhibition prevailed over excitation in CA2 (EPSP/IPSP < 1) (Fig. 3D).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
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In the paper
“With inhibition intact, LIII stimulation produced a net hyperpolarization and failed to elicit a spike in CA1 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
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In the paper
“Following block of inhibition, the burst of LIII stimuli caused a larger depolarization that triggered spikes in 80% of CA2 neurons (n = 12/15) but remained subthreshold for nearly all CA1 neurons (only 1 in 12 fired a spike; Fig. 4C).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
plaindirectn = 12- Asserted: passes — The authors put it forward as true.
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In the paper
“The induction of LTP at LIII synapses in both CA1 and CA2 was blocked by the NMDA receptor antagonist APV, indicating these two processes share certain molecular mechanisms (Fig. S3A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Although LII and LIII EC inputs to CA2 terminate in close proximity in SLM, LTP was pathway specific because LIII EC inputs displayed only a small and transient increase in efficacy when the HFS was delivered to LII EC inputs (Fig. S4C).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
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In the paper
“LTP at the LII –CA2 synapses was not altered in slices in which the mossy fiber inputs were cut, or with DCG-IV present to block glutamate release from the mossy fiber terminals, indicating that the LTP did not require activation of CA3 neurons (Fig. S4B).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
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In the paper
“We confirmed that the large LTP of the fEPSP was actually due to potentiation of synaptic responses in CA2 pyramidal neurons using whole cell recordings (Fig. S3B, 158.7 ± 5.2%, n = 6).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
boosteddirectn = 6- Asserted: passes — The authors put it forward as true.
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In the paper
“Histograms of the EPSC amplitude distribution showed a prominent peak at 0 pA, representing the failures, and a broad distribution of EPSC successes clearly resolvable from the peak of failures.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
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- Rests on an assumption: Synaptic transmission at CA2–CA1 synapses is quantal.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“When activated together, LII and LIII EPSPs showed linear summation for small amplitude EPSPs, whereas larger amplitude EPSPs displayed sublinear summation (Fig. 6A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
plaincorrelationaln = 20- Asserted: passes — The authors put it forward as true.
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In the paper
“The LII EC synapses with CA2 neurons generated a correspondingly large LTP (194.3 ± 9.8% increase in the fEPSP, n = 6) that was more than two-fold greater than the amount of LTP at LII synapses in CA3 (135.1 ± 9.3%, n = 6, p = 0.0008, Fig. 7C).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
plaindirectn = 6- Asserted: passes — The authors put it forward as true.
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In the paper
“When stimulated at different intervals, the two inputs summated over a symmetrical time window that lasted around 20 ms and showed a maximum summation when activated simultaneously (Fig. 6B).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Finally, induction of LTP at the LIII inputs produced a large, ~250% increase in the amplitude of the CA2 population spike elicited by strong stimulation (Fig. S4A), indicating an enhancement in the efficiency with which cortical inputs drive CA2 firing.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Both LII and LIII synapses onto CA2 neurons express robust long-term potentiation
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“The probability of a CA2–CA1 EPSC success ranged between 0.4 and 0.6 (Fig. 8D), similar to the value at CA3–CA1 synapses (Bolshakov and Siegelbaum, 1995).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
What the sources say
- Not checked yetcites Bolshakov and Siegelbaum, 1995
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It may state two separate claims as one.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In addition, whereas a single peak of EPSC successes was reported for CA3–CA1 synapses, the CA2–CA1 EPSCs always showed multiple peaks of successes, which occurred at equally spaced intervals of around −5 pA (Fig. 8B).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
- Rests on an assumption: Synaptic transmission at CA2–CA1 synapses is quantal.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“First, whereas CA1 neurons have a large number of oblique secondary dendrites in SR that shunt the synaptic current as it propagates down the dendrite, CA2 neurons have very few oblique dendrites in SR.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Reversal of normal dendritic integration rules between CA1 and CA2 neurons
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- Rests on an assumption: Excitatory synaptic inputs terminating on distal dendrites usually provide weaker somatic drive than proximal inputs due to cable properties.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Although this residual hippocampal function was originally proposed to result from the ability of the direct connection from LIII EC neurons to drive the firing of CA1 neurons, such inputs generate weak EPSPs in the CA1 neuron soma, display little LTP, and recruit strong feed-forward inhibition that suppresses CA1 neuron output.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
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In the paper
“Here we report that hippocampal CA2 pyramidal neurons, whose function has remained obscure for 75 years, have a reversed synaptic strength rule. Thus, CA2 neurons are strongly excited by their distal dendritic inputs from entorhinal cortex but only weakly activated by their more proximal dendritic inputs from hippocampal CA3 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > Abstract
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In the paper
“CA2 neurons could be further distinguished from CA3 neurons in that CA2 (and CA1) neuron dendrites branch along the transverse axis of the hippocampus (parallel to the plane of the slice) whereas CA3 neurons mostly extend their dendrites along the longitudinal axis of the hippocampus (Ishizuka et al., 1995).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Characterization of CA2 pyramidal neurons
What the sources say
- Not checked yetcites Ishizuka et al., 1995 source
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
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In the paper
“In this manner CA2 neurons form the nexus of a highly plastic disynaptic circuit linking the cortical input to the hippocampus to its CA1 neuronal ouput.”
- Also stated in: § INTRODUCTION · plain
“Finally, CA2 neurons make unusually strong unitary connections with CA1 neurons, forming a potent disynaptic circuit, independent of the trisynaptic path, that is powerfully regulated by long-term synaptic plasticity.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > Abstract
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- Also stated in: § INTRODUCTION · plain
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In the paper
“LII EC axons form excitatory synapses on granule cells in the molecular layer of dentate gyrus (DG), then project onto the distal dendrites of CA3 neurons, and finally terminate in a U shaped-area near the distal dendrites of CA2 (Niimi et al., 2007; Nishimura-Akiyoshi et al., 2007; Tamamaki and Nojyo, 1995).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
What the sources say
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“This suggests that SC inputs on their own are strong enough to drive firing in CA2 pyramidal neurons, but their impact is tightly controlled by feed-forward inhibition.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LIII EC inputs drive firing in CA2 but not CA1 pyramidal neurons
hedgeddirectn = 6- Asserted: passes — The authors put it forward as true.
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In the paper
“The larger SC synaptic response in CA1 versus CA2 is consistent with the greater number of oblique dendritic branches in the SR of CA1 compared to CA2 neurons and the more extensive branching of CA3 axons in CA1 versus CA2, suggestive of a greater number of synaptic contacts.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
hedgedcorrelationaln = 8- Asserted: passes — The authors put it forward as true.
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In the paper
“The larger SC intracellular EPSP in CA1 versus CA2 neurons is likely to result from a larger excitatory synaptic current as the local fEPSP in the SR region of CA1 was larger than that in CA2 (Fig. 3B), despite similar fiber volleys in both areas (not shown).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Reversed synaptic drive of EC versus CA3 inputs onto CA1 and CA2 pyramidal neurons
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“This polysynaptic response likely resulted from the recruitment of the DG→CA3→CA2 pathway either by activation of LII inputs to granule cells or by their direct activation as it was blocked by the mGluR-II agonist DCG-IV, which produces potent presynaptic inhibition at the mossy fiber synapses from DG to CA3 neurons but does not alter SC EPSPs (Kamiya et al., 1996) (Fig. 5A).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
What the sources say
- Not checked yetcites Kamiya et al., 1996 source
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“These data are consistent with the known anatomical projections of LII and LIII EC axons and confirm that our stimulating electrodes in DG and CA1 specifically recruited LII and LIII inputs, respectively.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Anatomical reconstructions have shown that CA2 pyramidal neurons send their axons to both SR and stratum oriens (SO) of CA1 (Tamamaki et al., 1988), whereas ipsilateral CA3 neurons only send their axons to SR.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > Paired recordings demonstrate strong unitary CA2 CA1 synaptic connections
What the sources say
- Not checked yetcites Tamamaki et al., 1988 source
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“These results show that both LII and LIII converge onto CA2 neurons where they interact and exert their maximal effect throughout the hippocampus.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > RESULTS > LII and LIII EC neurons produce strong convergent excitation of CA2 pyramidal neurons
boosteddirectn = 20- Asserted: passes — The authors put it forward as true.
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In the paper
“Altogether, our findings in acute slices reveal that CA2 neurons are a major target of excitatory cortical input to the hippocampus and can potently excite their CA1 neuron targets.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“First, CA2 neurons receive uniquely strong, convergent excitatory input from LII and LIII EC neurons, the only site of such convergence in the hippocampus.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Third, both the LII and LIII synapses with CA2 neurons undergo strong LTP, enhancing the efficacy with which these inputs fire CA2 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“This inhibition is likely to be important in gating information flow between CA3 and CA2 and may explain why CA2 neurons do not normally mediate a significant quadrisynaptic loop from EC to DG to CA3 to CA2 to CA1.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
hedgedconditional- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“The relevance of this inhibitory drive is suggested by the findings that selective decreases in CA2 inhibition are associated with schizophrenia (Benes et al., 1998) and epilepsy (Williamson and Spencer, 1994), two pathological conditions in which hippocampal excitability is increased.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
What the sources say
- Not checked yetcites Benes et al., 1998 source
- Not checked yetcites Williamson and Spencer, 1994
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“The strong inhibition might also terminate CA2 neuron firing after its initial activation by the disynaptic loop, and thus prevent excessive activation of CA1 neurons.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
hedgedconditional- Asserted: passes — The authors put it forward as true.
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- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In contrast, the strong excitatory drive of the cortical inputs to CA2 neurons, combined with the unusually powerful unitary synaptic connection between CA2 and CA1 neurons, forms a robust disynaptic circuit that may be sufficient to drive CA1 neuron output to mediate key hippocampal functions in spatial learning and memory.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > CA2 synaptic properties ensure independent disynaptic and trisynaptic hippocampal loops
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Neurons were identified according to specific electrophysiological properties summarized in table 1.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > MATERIALS AND METHODS > Hippocampal slices
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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Probably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In contrast, the EC inputs to CA2 neurons are strong and undergo robust LTP that enhances the excitatory drive of the disynaptic path.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Thus the powerful excitatory disynaptic circuit linking EC to CA2 to CA1, combined with the marked feed-forward inhibition from CA3 to CA2, can explain how in vivo electrical stimulation of entorhinal cortex inputs leads to the initial firing of CA2 neurons, followed by firing of CA1 and then CA3 neurons (Bartesaghi and Gessi, 2004; Bartesaghi et al., 2006).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
What the sources say
- Not checked yetcites Bartesaghi and Gessi, 2004
- Not checked yetcites Bartesaghi et al., 2006 source
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Series resistance (typically 15–25 MΩ) was monitored throughout each experiment; cells with more than 15% change in series resistance were excluded from analysis.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > MATERIALS AND METHODS > Hippocampal slices
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“The location of the recorded neurons in CA2 was subsequently confirmed after fixation of the slice for 1 hour in 4% paraformaldehyde in phosphate buffer (PBS). We further confirmed the location in CA2 by staining the slice for α-actinin 2, a protein enriched in the CA2 area (Wyszynski et al., 1998)”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > MATERIALS AND METHODS > Anatomical identification of CA2 pyramidal neurons
What the sources say
- Not checked yetcites Wyszynski et al., 1998 source
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
In the paper
“This excitation may actually be enhanced upon lesion of CA3 due to the loss of feed-forward inhibition, providing a potential explanation for the elevated rate of CA1 neuron place cell firing in the lesioned animals (Nakashiba et al., 2008).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
What the sources say
- Not checked yetcites Nakashiba et al., 2008 source
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Finally, CA2 neurons are the only hippocampal target of the supramammillary nucleus (which also targets the dentate gyrus), a structure involved in controlling the frequency of the theta rhythm (Pan and McNaughton, 2002) and the spread of epileptic activity (Saji et al., 2000) in the hippocampus.”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
What the sources say
- Not checked yetcites Pan and McNaughton, 2002
- Not checked yetcites Saji et al., 2000 source
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Moreover, the disynaptic circuit can account for the residual hippocampal-dependent memory and high levels of CA1 place cell firing in vivo following surgical or genetic lesions of CA3 (Brun et al., 2002; Nakashiba et al., 2008).”
§ Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop > DISCUSSION > Potential physiological role of CA2 neurons
What the sources say
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
The paper relies on this without support.
CA2 pyramidal neuron function has remained obscure for 75 years.
“Here we report that hippocampal CA2 pyramidal neurons, whose function has remained obscure for 75 years, have a reversed synaptic strength rule.”
The paper relies on this without support.
The postsynaptic target of CA2 neurons has not been verified and a synaptic connection between CA2 and CA1 pyramidal neurons has never been reported.
“However, the postsynaptic target of CA2 neurons has not been verified and a synaptic connection between CA2 and CA1 pyramidal neurons has never been reported.”
The paper relies on this without support.
The CA2 region comprises a small population of neurons between CA3 and CA1.
“First characterized by (Lorente de No, 1934), the CA2 region comprises a small population of neurons between CA3 and CA1 whose function remains largely unexplored.”
The paper relies on this without support.
Most hippocampal neurons have weak unitary connections.
“Moreover, given the small number of CA2 neurons and the weak unitary connections between most hippocampal neurons, it is unclear how CA2 neuron input could elicit CA1 output.”
The paper relies on this without support.
Synaptic transmission at CA2–CA1 synapses is quantal.
“As expected for quantal synaptic transmission”
The paper relies on this without support.
Excitatory synaptic inputs terminating on distal dendrites usually provide weaker somatic drive than proximal inputs due to cable properties.
“Because of the cable properties of neuronal dendrites, excitatory synaptic inputs terminating on the distal regions of the dendritic tree usually provide a much weaker excitatory drive at the soma compared to inputs that terminate on more proximal regions of the dendritic tree.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“the electrophysiological properties of the YFP+ neurons differed significantly from those of CA1 PNs (Extended Data Table 1) and largely matched the values previously reported for CA2 pyramidal neurons7”
From The hippocampal CA2 region is essential for social memory (2014) · cites this paper as [7]
Citations
Cites
de Nó, R. L. (1934) · Cited by 1,974
The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782 · cited 1×
“Genetic approaches have demonstrated the importance of long-term potentiation of synaptic transmission (LTP) (Neves et al., 2008) at each stage of the trisynaptic circuit (McHugh et al., 2007; Otto et al., 2001; Tsien et al., 1996).”
Pyramidal neurons: dendritic structure and synaptic integration
Spruston, N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2286 · Cited by 1,688
Synaptic plasticity, memory and the hippocampus: a neural network approach to causality
Neves, G., Cooke, S. F., & Bliss, T. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2303 · Cited by 1,287
The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041
Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network
McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. (2007) · Science · doi:10.1126/science.1140263 · Cited by 958
Dendritic spikes as a mechanism for cooperative long-term potentiation
Golding, N. L., Staff, N. P., & Spruston, N. (2002) · Nature · doi:10.1038/nature00854 · Cited by 623
Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons
Magee, J. C. (1999) · Nature Neuroscience · doi:10.1038/9158 · Cited by 617
Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry
Brun, V. H., Otnæss, M. K., Molden, S., Steffenach, H.-A., Witter, M. P., Moser, M.-B., & Moser, E. I. (2002) · Science · doi:10.1126/science.1071089 · Cited by 606
Immunohistochemical localization of Ih channel subunits, HCN1–4, in the rat brain
Notomi, T., & Shigemoto, R. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.11039 · Cited by 558
Cited by
Sorted by citations
The hippocampal CA2 region is essential for social memory
Hitti, F. L., & Siegelbaum, S. A. (2014) · Nature · doi:10.1038/nature13028 · Cited by 976
Self-citationCell type–specific genetic and optogenetic tools reveal hippocampal CA2 circuits
Kohara, K., Pignatelli, M., Rivest, A. J., Jung, H.-Y., Kitamura, T., Suh, J., Frank, D., Kajikawa, K., Mise, N., Obata, Y., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3614 · Cited by 528
Jackson, A. C., & Nicoll, R. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.007 · Cited by 410
Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling
Fernández‐Ruiz, A., Oliva, A., Nagy, G. A., Maurer, A. P., Berényi, A., & Buzsáki, G. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.017 · Cited by 344
Rediscovering area CA2: unique properties and functions
Dudek, S. M., Alexander, G. M., & Farris, S. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.22 · Cited by 333
Metadata
- Authors
- Chevaleyre, V., & Siegelbaum, S. A.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Chevaleyre, Vivien
- Siegelbaum, Steven A.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2010-05
- Volume
- 66
- Issue
- 4
- Pages
- 560-572
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2905041
- OpenAlex
- W2079968698
- Semantic Scholar
- 74c42794d7b071743679598cdfc2c2006f247c7a
- Cited by
- 324
- References
- 52
- Citations by year
- 2026: 16 · 2025: 25 · 2024: 18 · 2023: 27 · 2022: 24 · 2021: 27 · 2020: 21 · 2019: 20 · 2018: 29 · 2017: 20 · 2016: 21 · 2015: 14 · 2014: 17 · 2013: 15 · 2012: 12
- FWCI
- 8.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1209 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute (MH80745)
- National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- hippocampal CA2, pyramidal neurons, synaptic efficacy, entorhinal cortex, CA3, CA1, synaptic plasticity, spatial memory, hippocampal circuitry
- MeSH terms
- Animals, Cerebral Cortex, Mice, Inbred C57BL, Neural Pathways, Synapses, Pyramidal Cells, Mice, CA2 Region, Hippocampal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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