Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence
Open accessAbstract
We found that optogenetic burst stimulation of hippocampal dopaminergic fibers from midbrain neurons in mice exploring novel environments enhanced the reactivation of pyramidal cell assemblies during subsequent sleep/rest. When applied during spatial learning of new goal locations, dopaminergic photostimulation improved the later recall of neural representations of space and stabilized memory performance. These findings reveal that midbrain dopaminergic neurons promote hippocampal network dynamics associated with memory persistence.
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TL;DR
Optogenetic burst activation of midbrain dopaminergic neurons or their hippocampal axons during novel exploration or spatial learning enhanced subsequent hippocampal sharp-wave/ripple reactivation and stabilized spatial memory in mice. The effect was D1/D5-receptor dependent and acted specifically on actively expressed neuronal assemblies.
Key findings
- Burst-mode photostimulation of VTA dopaminergic neurons or dCA1 dopaminergic axons during novel environment exploration enhanced subsequent hippocampal reactivation (VTA-ON: z=2.53, P=0.011; dCA1-ON: z=6.52, P=7.2×10−11), was blocked by the D1/D5 antagonist SCH23390, and was not observed in eYFP-only controls; tonic stimulation produced only a weak trend (z=1.94, P=0.052).
- In a crossword maze, dCA1-ON burst photostimulation during learning prevented degradation of memory performance in a 1-hour probe test (t23=4.99, P=4.8×10−5) without affecting learning performance (F19,405=0.40, P=0.99).
- Photostimulation promoted reinstatement of newly learned spatial maps in the probe test (z=5.90, P=3.6×10−9) and enhanced reactivation of firing patterns expressed during learning (z=3.16, P=0.0016), but not pre-learning patterns (z=0.21, P=0.84).
- VTA neurons increased firing in novel versus familiar environments (novelty-induced rate change=0.56±0.14 Hz, t156=3.88, P=0.00016) and showed a higher burst ratio (novelty-induced burst ratio change=0.31±0.07, t156=4.31, P=2.9×10−5). ChR2 targeting was specific: 98.6±0.4% of ChR2-expressing VTA neurons co-expressed TH, and 76±7% of TH-immunopositive neurons co-expressed ChR2-eYFP (n=4 mice).
Methods
- DAT-IRES-Cre mice received Cre-inducible ChR2-eYFP or eYFP control virus in VTA, with tetrode recordings in dorsal CA1 and optic fibers for VTA-ON or dCA1-ON photostimulation; open-field experiments used eight DATVTA::ChR2-eYFP mice and two DATVTA::eYFP controls (n=1363 dCA1 pyramidal neurons, 25510 cell pairs), and crossword-maze experiments used four DATVTA::ChR2-eYFP mice (560 dCA1 pyramidal cells, 12072 cell pairs).
- The crossword maze task included pre-learning, learning, rest, and probe stages; memory performance was measured by path length to the reward location, and PV-IRES-Cre mice (n=5) were used to test hippocampus dependency by disrupting local hippocampal network activity.
- Reactivation strength was measured as the Pearson correlation between theta co-firing during exploration and SWR co-firing during subsequent rest, with Fisher r-to-z transforms for comparisons; spatial rate maps and population map similarity were used to assess place-field and ensemble stability.
Limitations
- Stated: sample sizes were similar to those generally used in the field and were not pre-determined by a sample size calculation; data distributions for parametric tests were assumed normal but this was not formally tested.
- Stated: investigators were aware of each subject’s experimental condition, so blinding is not reported.
- Evident: the main optogenetic and maze experiments rely on small numbers of mice per condition (e.g., four mice for crossword-maze recordings, two eYFP controls), which limits generalization.
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- Findingown data
Optogenetic burst stimulation of hippocampal dopaminergic fibers from midbrain neurons in mice exploring novel environments enhanced the reactivation of pyramidal cell assemblies during subsequent sleep/rest.
“Here we found that optogenetic burst stimulation of hippocampal dopaminergic fibers from midbrain neurons in mice exploring novel environments enhanced the reactivation of pyramidal cell assemblies during subsequent sleep/rest.”
- Also stated in: § Abstract · plain
“We found that VTA-ON and dCA1-ON burst-mode photostimulation (Fig. 2a) during exploration of novel environments enhanced the subsequent reactivation of hippocampal waking firing patterns (Fig. 2b), without altering exploratory behavior or the arousal state in rest (Supplementary Figs. 3a-c,4).”
- Also stated in: § Abstract · plain
“Importantly we found that burst-mode photoactivation of dopaminergic neurons enhanced hippocampal reactivation further (VTA-ON: z=2.53, P=0.011; dCA1-ON: z=6.52, P=7.2×10−11; Fig. 2b) without altering the mean firing rate, spatial tuning or cross-environment reorganization of pyramidal assemblies (Supplementary Fig. 2).”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data
In DATVTA::ChR2-eYFP mice, 98.6±0.4% of ChR2-expressing VTA neurons co-expressed tyrosine hydroxylase.
“In these DATVTA::ChR2-eYFP mice, 98.6±0.4% of ChR2-expressing VTA neurons co-expressed tyrosine hydroxylase (TH), demonstrating a highly specific targeting of dopaminergic neurons, with 76±7% of TH-immunopositive neurons co-expressing ChR2-eYFP (n=4 mice; Fig. 1b).”
Quote in the paperSubstantial claim - Findingown data
Photostimulation during learning did not affect learning performance.
“Importantly, photostimulation during learning prevented the degradation of memory performance in a probe test held 1 hour later (t23 =4.99, P =4.8×10−5, t-test; Fig. 3b), despite not affecting learning performance (F19,405=0.40, P=0.99, ANOVA; Fig. 3b).”
Quote in the paperSubstantial claim - Findingown data
When applied during spatial learning of new goal locations, dopaminergic photostimulation stabilized memory performance.
“When applied during spatial learning of new goal locations, dopaminergic photostimulation improved the later recall of neural representations of space and stabilized memory performance.”
- Also stated in: § Abstract · plain
“Importantly, photostimulation during learning prevented the degradation of memory performance in a probe test held 1 hour later (t23 =4.99, P =4.8×10−5, t-test; Fig. 3b), despite not affecting learning performance (F19,405=0.40, P=0.99, ANOVA; Fig. 3b).”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingcitation
The distribution of transfected axons across brain areas was consistent with the known distribution of dopaminergic fibers.
“The distribution of transfected axons across brain areas was consistent with the known distribution of dopaminergic fibers37.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [37] Björklund, A. & Lindvall, O. in Handbook of Chemical Neuroanatomy, Volume 2: Classical Transmitters in the CNS, Part I (eds. Björklund, A. & Hökfelt, T.) 55–122 (Elsevier, 1984).
Not checked in the free run.
- Findingcitation
Firing associations between dCA1 pyramidal cells reorganized to represent each environment.
“Additionally, we confirmed that firing associations between dCA1 pyramidal cells reorganized to represent each environment2,4,5,17(Supplementary Fig. 2a).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [2] Wilson, M.A. & McNaughton, B.L. Science 261, 1055–1058 (1993). source
Not checked in the free run.
- cites [4] Kentros, C. et al. Science 280, 2121–2126 (1998). source
Not checked in the free run.
- cites [5] Frank, L.M., Stanley, G.B. & Brown, E.N. J. Neurosci. 24, 7681–7689 (2004). source
Not checked in the free run.
- Findingown data
Hippocampal firing patterns expressed during learning were more strongly reactivated in subsequent rest than the pre-learning patterns were in the rest after pre-learning exploration.
“Hippocampal firing patterns expressed during learning were more strongly reactivated in subsequent rest than the pre-learning patterns were in the rest after pre-learning exploration (z=4.23, P=2.3×10−5; Fig. 3e).”
Quote in the paperSubstantial claim - Findingown data
Photostimulation during learning did not extend its effect back to the patterns expressed during the pre-learning exploration.
“Photostimulation during learning further enhanced the reactivation of the concurrently expressed firing patterns (z=3.16, P=0.0016; Fig. 3e), but did not extend its effect back to the patterns expressed during the pre-learning exploration (z=0.21, P=0.84; Fig. 3e).”
Quote in the paperSubstantial claim - Findingown data
Hippocampal patterns representing novel environments were more strongly reactivated in post-exploration SWRs than the old, well-established ones mapping the familiar environment.
“Moreover, hippocampal patterns representing novel environments were more strongly reactivated in post-exploration SWRs than the old, well-established ones mapping the familiar environment (z=4.79, P=1.7×10−6; Fig. 2b and Supplementary Table 3).”
Quote in the paperSubstantial claim - Findingown data
The persistence of memories was associated with the strength of hippocampal reactivation.
“The persistence of memories was associated with the strength of hippocampal reactivation.”
Quote in the paperSubstantial claim - Findingown data
In non-photostimulated sessions, the firing rate of VTA neurons increased in novel environments compared to familiar ones.
“In these non-photostimulated sessions we found that the firing rate of VTA neurons (n=157) increased in novel environments compared to the familiar ones (novelty-induced rate change=0.56±0.14Hz, t156=3.88, P=0.00016, paired t-test; Fig. 1e,f and Supplementary Fig. 1).”
Quote in the paperSubstantial claim - Findingown data
Tonic-mode stimulation consisting of the same number of light pulses produced only a weak trend of increased reactivation.
“Furthermore, tonic-mode stimulation consisting of the same number of light pulses (now equally spaced) produced only a weak trend of increased reactivation (z=1.94, P=0.052; Fig. 2b).”
Quote in the paperSubstantial claim - Findingown data
Enhanced reactivation was blocked by the D1/D5 antagonist SCH23390 injected prior to exploration.
“Such enhanced reactivation was blocked by the D1/D5 antagonist SCH23390 injected prior to exploration and was not observed in control mice transfected with a construct coding for the eYFP only (Fig. 2b and Supplementary Table 3).”
Quote in the paperSubstantial claim- Rests on an assumption: SCH23390 is a selective and potent antagonist of D1/D5 dopaminergic receptors.
- Findingown data
Axons co-expressing ChR2-eYFP and TH were found extending along the antero-posterior axis of the CA1 region of dorsal hippocampus with collaterals in the strata radiatum, pyramidale and oriens.
“In addition to their presence in other brain areas such as the striatum axons co-expressing ChR2-eYFP and TH were found extending along the antero-posterior axis of the CA1 region of dorsal hippocampus (dCA1) with collaterals in the strata radiatum, pyramidale and oriens (Fig. 1c,d).”
Quote in the paperSubstantial claim - Findingown data
Enhanced reactivation was not observed in control mice transfected with a construct coding for eYFP only.
“Such enhanced reactivation was blocked by the D1/D5 antagonist SCH23390 injected prior to exploration and was not observed in control mice transfected with a construct coding for the eYFP only (Fig. 2b and Supplementary Table 3).”
Quote in the paperSubstantial claim - Findingown data
In DATVTA::ChR2-eYFP mice, 76±7% of TH-immunopositive neurons co-expressed ChR2-eYFP.
“In these DATVTA::ChR2-eYFP mice, 98.6±0.4% of ChR2-expressing VTA neurons co-expressed tyrosine hydroxylase (TH), demonstrating a highly specific targeting of dopaminergic neurons, with 76±7% of TH-immunopositive neurons co-expressing ChR2-eYFP (n=4 mice; Fig. 1b).”
Quote in the paperSubstantial claim - Findingown data
Behavioral performance gradually improved with learning trials, as measured by a shortening of distance travelled from start-box to reward in each trial.
“Behavioral performance gradually improved with learning trials, as measured by a shortening of distance travelled from start-box to reward in each trial (Fig. 3a,b).”
Quote in the paperNot a substantial claim - Findingown data
Photostimulation during learning further enhanced the reactivation of the concurrently expressed firing patterns.
“Photostimulation during learning further enhanced the reactivation of the concurrently expressed firing patterns (z=3.16, P=0.0016; Fig. 3e), but did not extend its effect back to the patterns expressed during the pre-learning exploration (z=0.21, P=0.84; Fig. 3e).”
Quote in the paperSubstantial claim - Findingown data
When applied during spatial learning of new goal locations, dopaminergic photostimulation improved the later recall of neural representations of space.
“When applied during spatial learning of new goal locations, dopaminergic photostimulation improved the later recall of neural representations of space and stabilized memory performance.”
- Also stated in: § Abstract · plain
“However, the reinstatement of the newly-learned spatial maps in the probe test was promoted following activation of dCA1 dopaminergic axons (z=5.90, P=3.6×10−9; Fig. 3d), a phenomenon associated with memory recall6.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [6] Dupret, D., O'Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. Nat. Neurosci. 13, 995–1002 (2010). source
Not checked in the free run.
- Also stated in: § Abstract · plain
- Findingown data
For all conditions, reactivation strength was higher than in a baseline comparison with SWR patterns from the initial rest before all exploration.
“For all conditions, reactivation strength (the correlation of the waking theta co-firing patterns with subsequent rest SWR co-firing patterns) was higher than in a baseline comparison with SWR patterns from the initial rest before all exploration (all P<0.0001; Fig. 2b, white versus gray bars; Supplementary Table 2).”
Quote in the paperSubstantial claim - Findingown data
The reorganization of hippocampal spatial maps between the pre-learning and the learning periods was unaffected by photostimulation.
“The reorganization of hippocampal spatial maps between the pre-learning and the learning periods was also unaffected by photostimulation (Fig. 3c,d and Supplementary Fig. 7).”
Quote in the paperNot a substantial claim - Findingown data
The VTA firing response to spatial novelty resulted in a higher fraction of action potentials discharged in bursts.
“This VTA firing response to spatial novelty, which might be partially informed by hippocampal spatio-contextual inputs10,16, resulted in a higher fraction of action potentials discharged in bursts (interspike interval<50ms; novelty-induced burst ratio change=0.31±0.07, t156=4.31, P=2.9×10−5, paired t-test), a potentially suitable signal to in turn modulate hippocampal dynamics.”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
New representations formed during exploration of novel environments or learning of new goal locations are initially labile and require stabilization to persist as memories.
“However new representations, such as those formed during exploration of novel environments or learning of new goal locations, are initially labile and thus require stabilization to persist as memories4-6.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [4] Kentros, C. et al. Science 280, 2121–2126 (1998). source
Not checked in the free run.
- cites [5] Frank, L.M., Stanley, G.B. & Brown, E.N. J. Neurosci. 24, 7681–7689 (2004). source
Not checked in the free run.
- cites [6] Dupret, D., O'Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. Nat. Neurosci. 13, 995–1002 (2010). source
Not checked in the free run.
- Interpretationown data
Our findings demonstrate that dopaminergic activity at the time of formation of new hippocampal cell assemblies increases the subsequent off-line SWR reactivation of these assemblies.
“Our findings demonstrate that dopaminergic activity at the time of formation of new hippocampal cell assemblies increases the subsequent off-line SWR reactivation of these assemblies.”
Quote in the paperSubstantial claim - Interpretationown data
This is consistent with the hypothesis that SWR reactivation supports the consolidation of newly-formed neuronal assemblies.
“This is consistent with the hypothesis that SWR reactivation supports the consolidation of newly-formed neuronal assemblies17.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [17] O'Neill, J., Senior, T.J., Allen, K., Huxter, J.R. & Csicsvari, J. Nat. Neurosci. 11, 209–215 (2008). source
Not checked in the free run.
- Interpretationown data
These findings reveal that midbrain dopaminergic neurons promote hippocampal network dynamics associated with memory persistence.
“These findings reveal that midbrain dopaminergic neurons promote hippocampal network dynamics associated with memory persistence.”
Quote in the paperSubstantial claim - Premisecitation
Blockade of D1/D5 dopaminergic receptors during exploration of novel environments curtails the stability of new spatial maps.
“while blockade during exploration of novel environments curtails the stability of new spatial maps8”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [8] Kentros, C.G., Agnihotri, N.T., Streater, S., Hawkins, R.D. & Kandel, E.R. Neuron 42, 283–295 (2004). source
Not checked in the free run.
- Interpretationown data
Our results provide novel insights into the relationship between midbrain dopaminergic neurons, encoding salient information about an environment, and hippocampal assemblies, providing representations of space, in modulating memory according to the value of the information to be remembered.
“Our results thus provide novel insights into the relationship between midbrain dopaminergic neurons, encoding salient information about an environment9,10,16,19,20, and hippocampal assemblies, providing representations of space1-3, in modulating memory according to the value of the information to be remembered.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [9] Li, S., Cullen, W.K., Anwyl, R. & Rowan, M.J. Nat. Neurosci. 6, 526–531 (2003). source
Not checked in the free run.
- cites [10] Lisman, J.E. & Grace, A.A. Neuron 46, 703–713 (2005). source
Not checked in the free run.
- cites [16] Luo, A.H., Tahsili-Fahadan, P., Wise, R.A., Lupica, C.R. & Aston-Jones, G. Science 333, 353–357 (2011). source
Not checked in the free run.
- Interpretationown data
This finding indicates that dopamine acts specifically on actively expressed neuronal assemblies.
“This finding indicates that dopamine acts specifically on actively expressed neuronal assemblies.”
Quote in the paperSubstantial claim - Premisecitation
Electrical disruption of SWRs after learning impairs spatial memory.
“Indeed, electrical disruption of SWRs after learning impairs spatial memory13.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [13] Girardeau, G., Benchenane, K., Wiener, S.I., Buzsáki, G. & Zugaro, M.B. Nat. Neurosci. 12, 1222–1223 (2009). source
Not checked in the free run.
- Premisecitation
In the hippocampus, memory stabilization is thought to be supported by sleep reactivation, whereby assembly firing patterns expressed during exploration are reactivated in subsequent sleep/rest periods during sharp wave/ripple oscillatory events.
“In the hippocampus memory stabilization is thought to be supported by ‘sleep reactivation’ whereby assembly firing patterns expressed during exploration are reactivated in subsequent sleep/rest periods during sharp wave/ripple (SWR, 135–250Hz) oscillatory events11,12.”
Quote in the paperSubstantial claim0 of 2 sources checked - Interpretationown data
Collectively these data demonstrate that burst-mode activation of dopaminergic neurons increases hippocampal reactivation in a D1/D5 receptor dependent manner.
“Collectively these data demonstrate that burst-mode activation of dopaminergic neurons increases hippocampal reactivation in a D1/D5 receptor dependent manner.”
Quote in the paperSubstantial claim- Rests on an assumption: SCH23390 is a selective and potent antagonist of D1/D5 dopaminergic receptors.
- Interpretationown data
These data highlight the structural substrate by which midbrain-derived dopamine could modulate hippocampal dynamics.
“In line with earlier reports these data highlight the structural substrate by which midbrain-derived dopamine could modulate hippocampal dynamics10,15.”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
Pharmacological studies have implicated the neurotransmitter dopamine in the stability of hippocampus-dependent memory.
“Pharmacological studies have implicated the neurotransmitter dopamine in the stability of hippocampus-dependent memory.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [7] Bethus, I., Tse, D. & Morris, R.G.M. J. Neurosci. 30, 1610–1618 (2010). source
Not checked in the free run.
- cites [8] Kentros, C.G., Agnihotri, N.T., Streater, S., Hawkins, R.D. & Kandel, E.R. Neuron 42, 283–295 (2004). source
Not checked in the free run.
- cites [9] Li, S., Cullen, W.K., Anwyl, R. & Rowan, M.J. Nat. Neurosci. 6, 526–531 (2003). source
Not checked in the free run.
- Premisecitation
Blockade of D1/D5 dopaminergic receptors during spatial learning impairs memory persistence.
“Blockade of D1/D5 dopaminergic receptors during spatial learning impairs memory persistence7”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [7] Bethus, I., Tse, D. & Morris, R.G.M. J. Neurosci. 30, 1610–1618 (2010). source
Not checked in the free run.
- May combine two claims. 8
- Classified as probably not a substantial claim. 17
- The quote only partly states this claim. 1
May combine two claims.
Findingown dataBurst-mode photoactivation of dopaminergic neurons did not alter the mean firing rate, spatial tuning or cross-environment reorganization of pyramidal assemblies.
“Importantly we found that burst-mode photoactivation of dopaminergic neurons enhanced hippocampal reactivation further (VTA-ON: z=2.53, P=0.011; dCA1-ON: z=6.52, P=7.2×10−11; Fig. 2b) without altering the mean firing rate, spatial tuning or cross-environment reorganization of pyramidal assemblies (Supplementary Fig. 2).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Findingown dataThe mean number of theta cycles per waking session used for spike binning did not differ across conditions in open field experiments (F3,143=1.41, P=0.24, ANOVA) and in crossword maze experiments (t23=1.31, P=0.20, t-test).
“The mean number of theta cycles per waking session used for spike binning was not different across conditions (open field experiments: 5699.6±165.5, F3,143=1.41, P=0.24, ANOVA; crossword maze experiments=15038.5±855.6, t23=1.31, P=0.20, t-test; mean±s.e.m.).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: Data distributions for parametric tests are normal.
May combine two claims.
Findingown dataVTA-ON and dCA1-ON burst-mode photostimulation during exploration of novel environments did not alter exploratory behavior or the arousal state in rest.
“We found that VTA-ON and dCA1-ON burst-mode photostimulation (Fig. 2a) during exploration of novel environments enhanced the subsequent reactivation of hippocampal waking firing patterns (Fig. 2b), without altering exploratory behavior or the arousal state in rest (Supplementary Figs. 3a-c,4).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). The quote only partly states this claim.
Findingnone givenUse of an 80ms cut-off for burst classification produced similar findings to the 50ms cut-off.
“Note that use of a 80ms cut-off produced similar findings.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataDetected theta windows corresponded to periods when the animals were actively exploring the environment.
“These detected theta windows corresponded to periods when the animals were actively exploring the environment (Supplementary Fig. 3d).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataNeither the mean firing rate nor the proportion of spiking pyramidal cells during SWRs were changed.
“Neither the mean firing rate nor the proportion of spiking pyramidal cells during SWRs were changed (Supplementary Fig. 5).”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
PremisecitationBlockade of D1/D5 dopaminergic receptors during exploration of novel environments prevents novelty-facilitated synaptic plasticity.
“and also prevents novelty-facilitated synaptic plasticity9.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [9] Li, S., Cullen, W.K., Anwyl, R. & Rowan, M.J. Nat. Neurosci. 6, 526–531 (2003). source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe random assignment of each subject to the various experimental conditions is reported in Supplementary Table 1.
“All recordings were performed during day time and the random assignment of each subject to the various experimental conditions is reported in Supplementary Table 1.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
PremisecitationSuch reactivation is thought to enable the incorporation of new memory engrams, especially those associated with novel and rewarded outcomes, into stable representations capable of informing future behavior.
“Such reactivation is thought to enable the incorporation of new memory engrams, especially those associated with novel and rewarded outcomes, into stable representations capable of informing future behavior6,11,12,18.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [6] Dupret, D., O'Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. Nat. Neurosci. 13, 995–1002 (2010). source
Not checked in the free run.
- cites [11] Buzsáki, G. Neuroscience 31, 551–570 (1989). source
Not checked in the free run.
- cites [12] Wilson, M.A. & McNaughton, B. Science 265, 676–679 (1994). source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenInvestigators were aware as to which experimental conditions each subject had to be exposed to.
“Investigators were aware as to which experimental conditions each subject had to be exposed to (e.g., Familiar versus Novel, Photostimulation OFF versus ON, Exploration versus Sleep).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.
Study design and conductnone givenSample sizes in this study are similar to those generally employed in the field and were not pre-determined by a sample size calculation.
“Sample sizes in this study are similar to those generally employed in the field and were not pre-determined by a sample size calculation.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe board was cleaned after each learning trial to discourage the use of an odor guided search strategy.
“The board was cleaned after each learning trial to discourage the use of an odor guided search strategy.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Study design and conductnone givenIn all experiments, each mouse alternated between days with photostimulation OFF and days with photostimulation ON.
“In all of these experiments each mouse alternated between days with photostimulation OFF and days with photostimulation ON.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenData distributions for parametric tests were assumed to be normal but this was not formally tested.
“Data distributions for parametric tests were assumed to be normal but this was not formally tested.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
PremisecitationThe contribution of dopamine towards hippocampal neuronal dynamics associated with memory persistence remains to be identified.
“However the contribution of dopamine towards hippocampal neuronal dynamics associated with memory persistence remains to be identified10.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [10] Lisman, J.E. & Grace, A.A. Neuron 46, 703–713 (2005). source
Not checked in the free run.
Classified as probably not a substantial claim.
PremisecitationBrain representations of space are encoded by pyramidal cell assemblies in the hippocampus during active behavior.
“Brain representations of space are encoded by pyramidal cell assemblies in the hippocampus during active behavior1-3.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [1] O'Keefe, J. Exp. Neurol. 51, 78–109 (1976). source
Not checked in the free run.
- cites [2] Wilson, M.A. & McNaughton, B.L. Science 261, 1055–1058 (1993). source
Not checked in the free run.
- cites [3] Moser, E.I., Kropff, E. & Moser, M.B. Annu. Rev. Neurosci. 31, 69–89 (2008). source
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
Study design and conductcitationUnits were deemed independent from each other by their distinct spike waveform, the absence of refractory period in their cross-correlations and separable principal component boundaries using a measure based on the Mahalanobis distance.
“Units were deemed independent from each other by i) their distinct spike waveform, ii) the absence of refractory period in their cross-correlations and iii) separable principal component boundaries using a measure based on the Mahalanobis distance24,26.”
Quote in the paperSubstantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductreasoningThe maze was randomly rotated relative to the cues at the beginning of each day in order to promote allocentric spatial navigation by distal cues.
“In order to promote allocentric spatial navigation by distal cues, the maze was randomly rotated relative to the cues at the beginning of each day.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim. May combine two claims.
Study design and conductreasoningOnly well-isolated and stable units over the entire recording day were used for further analysis; namely units that showed a clear refractory period in their auto-correlations and well-defined cluster boundaries across all recording sessions of the day.
“Only well-isolated and stable units over the entire recording day were used for further analysis; namely units that showed a clear refractory period in their auto-correlations and well-defined cluster boundaries across all recording sessions of the day.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductcitationHippocampal pyramidal cells were identified by their auto-correlogram, firing rate and spike waveform, as previously described.
“Hippocampal pyramidal cells were identified by their auto-correlogram, firing rate and spike waveform, as previously described24.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [24] Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A. & Buzsáki, G. J. Neurosci. 19, 274–287 (1999). source
Not checked in the free run.
The paper relies on this without support.
The crossword maze task is hippocampus-dependent.
“trained to a hippocampus-dependent learning task on a crossword-like maze”
The paper relies on this without support.
SCH23390 is a selective and potent antagonist of D1/D5 dopaminergic receptors.
“SCH23390, a selective and potent antagonist of D1/D5 dopaminergic receptors (Sigma, #D054; 0.1mg/kg in 0.9% saline, i.p.)”
The authors state this as an assumption.
Data distributions for parametric tests are normal.
“Data distributions for parametric tests were assumed to be normal but this was not formally tested.”
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?
Ventral tegmental area-hippocampal DA projections likely stabilize memory of searching for a spatial goal.
“they likely stabilize memory of searching for a spatial goal”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as McNamara et al., 2014
Despite the sparse innervation of the hippocampus by midbrain dopaminergic axons, several lines of evidence indicate a significant functional role for this dopaminergic innervation.
“Despite the sparse innervation of the hippocampus by midbrain dopaminergic axons, several lines of evidence indicate a significant functional role for this dopaminergic innervation.”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as McNamara et al., 2014
Our results confirm recent studies using viral expression of channelrhodopsin in Slc6a3ires-cre/+ mice that labeled relatively sparse dopaminergic axons in the CA1 region.
“Our results also confirm recent studies using viral expression of channelrhodopsin in Slc6a3ires-cre/+ mice that labeled relatively sparse dopaminergic axons in the CA1 region (McNamara et al., 2014; Rosen et al., 2015).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as McNamara et al., 2014
Optical stimulation of dopaminergic fibers in the VTA or locally in the hippocampus in mice exploring novel environments enhanced hippocampal reactivation and improved spatial learning and memory.
“Optical stimulation of these dopaminergic fibers in the VTA or locally in the hippocampus in mice exploring novel environments enhanced hippocampal reactivation and improved spatial learning and memory (McNamara et al., 2014).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as McNamara et al., 2014
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Consistentz = 2.53reported p = .011 · recomputed p = .011
“z=2.53, p = .011”
- Consistentz = 1.94reported p = .052 · recomputed p = .052
“(z=1.94, p = .052”
- Consistentz = 3.16reported p = .0016 · recomputed p = .002
“(z=3.16, p = .0016”
- Consistentz = 0.21reported p = .84 · recomputed p = .834
“(z=0.21, p = .84”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Self-check results appear here once an independent check has confirmed them.
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“This conclusion is consistent with the hypothesis that DA signals under these circumstances contribute to the updating of the rodent’s internal perception (or map) of environmental saliency (Bethus et al., 2010; McNamara et al., 2014).”
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- Authors
- McNamara, C. G., Tejero-Cantero, Á., Trouche, S., Campo-Urriza, N., & Dupret, D.
- Affiliations
- University of Oxford (GB)
- Venue
- Nature Neuroscience
- Published
- 2014-10-19
- Volume
- 17
- Issue
- 12
- Pages
- 1658-1660
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4241115
- OpenAlex
- W2017814058
- Semantic Scholar
- 3430ac2912958b455b853e0424bc5509f7ff4d67
- Cited by
- 486
- References
- 39
- Citations by year
- 2026: 26 · 2025: 34 · 2024: 69 · 2023: 48 · 2022: 42 · 2021: 42 · 2020: 43 · 2019: 32 · 2018: 51 · 2017: 42 · 2016: 37 · 2015: 18 · 2014: 2
- FWCI
- 18.41
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- dopaminergic neurons, midbrain dopamine, hippocampus, hippocampal reactivation, spatial memory, memory persistence, sleep, optogenetic stimulation, spatial learning, memory consolidation
- MeSH terms
- Animals, Hippocampus, Male, Mesencephalon, Mice, Transgenic, Neural Pathways, Random Allocation, Spatial Behavior, Maze Learning, Mice, Dopaminergic Neurons, Spatial Memory
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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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