Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology

Hasselmo, ME; Schnell, E

doi:10.1523/jneurosci.14-06-03898.1994

Cited by 466Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology

Open access

Hasselmo, ME, Schnell, E·1994·The Journal of Neuroscience

DOI 10.1523/jneurosci.14-06-03898.1994PMC PMC6576918

Open this paper in CoChat — free account

Abstract

ACh may set the dynamics of cortical function to those appropriate for learning new information. In models of the putative associative memory function of piriform cortex, selective suppression of intrinsic but not afferent fiber synaptic transmission by ACh prevents recall of previous input from interfering with the learning of new input (Hasselmo, 1993). Selective cholinergic suppression may play a similar role in the hippocampal formation, where Schaffer collateral synapses in stratum radiatum (s. rad) may store associations between activity in region CA3 and the entorhinal cortex input to region CA1 terminating in stratum lacunosum-moleculare (s. l-m). A computational model of region CA1 predicts that for effective associative memory function of the Schaffer collaterals, cholinergic suppression of synaptic transmission should be stronger in s. rad than in s. l-m. In the hippocampal slice preparation, we tested the effect of the cholinergic agonist carbachol (0.01–500 microM) on synaptic transmission in s. rad and s. l-m. Stimulating and recording electrodes were simultaneously placed in both layers, allowing analysis of the effect of carbachol on synaptic potentials in both layers during the same perfusion in each slice. Carbachol produced a significantly stronger suppression of stimulus- evoked EPSPs in s. rad than in s. l-m at all concentrations greater than 1 microM. At 100 microM, EPSP initial slopes were suppressed by 89.1 +/- 3.0% in s. rad, but only by 40.1 +/- 4.1% in s. l-m. The muscarinic antagonist atropine (1 microM) blocked cholinergic suppression in both layers. These data support the hypothesis that synaptic modification of the Schaffer collaterals may store associations between activity in region CA3 and the afferent input to region CA1 from the entorhinal cortex. In simulations, feedback regulation of cholinergic modulation based on activity in region CA1 sets the appropriate dynamics of learning for novel associations, and recall for familiar associations.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.14-06-03898.1994

Cites

83 of 83 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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 CA1 region of the hippocampus, long-range perforant inputs from the entorhinal cortex are less inhibited by acetylcholine than the Schaeffer collaterals arising from CA3.
“Indeed, in the CA1 region of the hippocampus, long-range perforant inputs from the entorhinal cortex are less inhibited by ACh than the Schaeffer collaterals arising from CA3 (Hasselmo and Schnell, 1994).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Hasselmo and Schnell, 1994
During encoding, the synapses being modified must not influence their postsynaptic target, to avoid distorting the stored representation.
“During encoding the synapses being modified must not influence their postsynaptic target, to avoid distorting the stored representation (Hasselmo and Bower, 1992, 1993; Hasselmo and Schnell, 1994).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Hasselmo and Schnell, 1994

Self-Organization and Associative Memory
Kohonen, T. (1989) · Springer Series in Information Sciences · doi:10.1007/978-3-642-88163-3 · Cited by 8,740 · see citing works
Simple memory: a theory for archicortex
Marr, D. (1971) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1971.0078 · Cited by 2,771 · see citing works
Modeling Brain Function
Amit, D. J. (1989) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623257 · Cited by 2,279 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system.
de Nó, R. L. (1934) · Cited by 1,974 · see citing works
Self-organization in a perceptual network
Linsker, R. (1988) · Computer · doi:10.1109/2.36 · Cited by 1,454 · see citing works
Self-organization of orientation sensitive cells in the striate cortex
Malsburg, C. V. D. (1973) · Kybernetik · doi:10.1007/bf00288907 · Cited by 1,444 · see citing works
Hippocampal synaptic enhancement and information storage within a distributed memory system
McNaughton, B. L., & Morris, R. G. M. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90011-7 · Cited by 1,304 · see citing works
The connections of the septal region in the rat
Swanson, L. W., & Cowan, W. M. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901860408 · Cited by 1,136 · see citing works
Correlation Matrix Memories
Kohonen, T. (1972) · IEEE Transactions on Computers · doi:10.1109/tc.1972.5008975 · Cited by 885 · see citing works
Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat
Steward, O. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901670303 · Cited by 883 · see citing works
Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat
Steward, O., & Scoville, S. A. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901690306 · Cited by 837 · see citing works
Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro.
Madison, D. V., & Nicoll, R. A. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015378 · Cited by 746 · see citing works
Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state
Huerta, P. T., & Lisman, J. E. (1993) · Nature · doi:10.1038/364723a0 · Cited by 564 · see citing works
Hebbian synapses in hippocampus.
Kelso, S. R., Ganong, A. H., & Brown, T. H. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.14.5326 · Cited by 555 · see citing works
A simple neural network generating an interactive memory
Anderson, J. A. (1972) · Mathematical Biosciences · doi:10.1016/0025-5564(72)90075-2 · Cited by 553 · see citing works
Hippocampal mediation of stimulus representation: A computational theory
Gluck, M. A., & Myers, C. E. (1993) · Hippocampus · doi:10.1002/hipo.450030410 · Cited by 496 · see citing works
Chunking and consolidation: A theoretical synthesis of semantic networks, configuring in conditioning, S-R versus cognitive learning, normal forgetting, the amnesic syndrome, and the hippocampal arousal system.
Wickelgren, W. A. (1979) · Psychological Review · doi:10.1037/0033-295x.86.1.44 · Cited by 494 · see citing works
Acetylcholine and memory
Hasselmo, M. E., & Bower, J. M. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90159-j · Cited by 429 · see citing works
Self-citation
Physiological mechanisms underlying long-term potentiation
Gustafsson, B., & Wigström, H. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90142-7 · Cited by 398 · see citing works
Cortical projection patterns of the medial septum‐diagonal band complex
Gaykema, R. P. A., Luiten, P. G. M., Nyakas, C. J., & Traber, J. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902930109 · Cited by 387 · see citing works
Modeling Brain Function: The World of Attractor Neural Networks
de Callataÿ, A. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90155-4 · Cited by 361 · see citing works
Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex
Hasselmo, M. E., & Bower, J. M. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.5.1222 · Cited by 358 · see citing works
Self-citation
Presynaptic inhibitory effect of acetylcholine in the hippocampus
Valentino, R. J., & Dingledine, R. J. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-07-00784.1981 · Cited by 340 · see citing works
Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex
Bland, B. H., & Colom, L. V. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90007-f · Cited by 321 · see citing works
Micromolar L-2-amino-4-phosphonobutyric acid selectively inhibits perforant path synapses from lateral entorhinal cortex
Koerner, J. F., & Cotman, C. W. (1981) · Brain Research · doi:10.1016/0006-8993(81)91288-9 · Cited by 304 · see citing works
Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca complex
Tóth, K., Borhegyi, Z., & Freund, T. F. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03712.1993 · Cited by 296 · see citing works
Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice.
Pitler, T. A., & Alger, B. E. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019119 · Cited by 288 · see citing works
Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway.
Yeckel, M. F., & Berger, T. W. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.15.5832 · Cited by 286 · see citing works
Hippocampal long‐term potentiation is induced by pairing single afferent volleys with intracellular^ injected depolarizing current pulses
Wigström, H., Gustafsson, B., Huang, Y.-Y., & Abraham, W. C. (1986) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1986.tb07822.x · Cited by 284 · see citing works
Cholinergic and GABAergic modulation of medial septal area: Effect on working memory.
Givens, B. S., & Olton, D. S. (1990) · Behavioral Neuroscience · doi:10.1037//0735-7044.104.6.849 · Cited by 279 · see citing works
Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex
Bröcher, S., Artola, A., & Singer, W. (1992) · Brain Research · doi:10.1016/0006-8993(92)90110-u · Cited by 272 · see citing works
Cholinergic and GABAergic modulation of medial septal area: Effect on working memory.
Givens, B. S., & Olton, D. S. (1990) · Behavioral Neuroscience · doi:10.1037/0735-7044.104.6.849 · Cited by 270 · see citing works
Cholinergic modulation of cortical associative memory function
Hasselmo, M. E., Anderson, B. P., & Bower, J. M. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.5.1230 · Cited by 250 · see citing works
Self-citation
Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells
Benardo, L. S., & Prince, D. A. (1982) · Brain Research · doi:10.1016/0006-8993(82)90067-1 · Cited by 246 · see citing works
Cortical oscillations and temporal interactions in a computer simulation of piriform cortex
Wilson, M. A., & Bower, J. M. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.4.981 · Cited by 234 · see citing works
Normal and amnesic learning, recognition and memory by a neural model of cortico-hippocampal interactions
Carpenter, G. A., & Grossberg, S. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90118-6 · Cited by 229 · see citing works
A Computational Approach to Hippocampal Function
Levy, W. B. (1989) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)60113-9 · Cited by 228 · see citing works
Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus
Mizumori, S., McNaughton, B. L., Barnes, C. A., & Fox, K. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03915.1989 · Cited by 223 · see citing works
Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus
Hounsgaard, J. (1978) · Experimental Neurology · doi:10.1016/0014-4886(78)90284-4 · Cited by 221 · see citing works
Organization of the septal region in the rat brain: Cholinergic‐GABAergic interconnections and the termination of hippocampo‐septal fibers
Léránth, C., & Frotscher, M. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890210 · Cited by 220 · see citing works
The Cholinergic Hypothesis of Memory: A Review of Animal Experiments
Hagan, J. J., & Morris, R. (1988) · Springer eBooks · doi:10.1007/978-1-4613-0933-8_7 · Cited by 213 · see citing works
Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway
Witter, M. P., Griffioen, A. W., Jorritsma-Byham, B., & Krijnen, J. L. M. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90350-3 · Cited by 212 · see citing works
Excitatory Synapses on Hippocampal Apical Dendrites Activated by Entorhinal Stimulation
Andersen, P. N., Holmqvist, B., & Voorhoeve, P. E. (1966) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1966.tb03224.x · Cited by 205 · see citing works
Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus
Blitzer, R. D., Gil, O., & Landau, E. M. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90835-w · Cited by 192 · see citing works
The hippocampal control of neuronal discharges in the septum of the rat
McLennan, H., & Miller, J. J. (1974) · The Journal of Physiology · doi:10.1113/jphysiol.1974.sp010500 · Cited by 191 · see citing works
Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus
Burgard, E. C., & Sarvey, J. M. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90382-j · Cited by 188 · see citing works
The Cholinergic Neurotransmitter System in Human Memory and Dementia: A Review
Kopelman, M. D. (1986) · The Quarterly Journal of Experimental Psychology Section A · doi:10.1080/14640748608401614 · Cited by 181 · see citing works
Reinnervation of the hippocampal perforant pathway zone in Alzheimer's disease
Hyman, B. T., Kromer, L. J., & van Hoesen, G. W. (1987) · Annals of Neurology · doi:10.1002/ana.410210307 · Cited by 177 · see citing works
On the development of feature detectors in the visual cortex with applications to learning and reaction-diffusion systems
Grossberg, S. (1976) · Biological Cybernetics · doi:10.1007/bf00337422 · Cited by 175 · see citing works
Baclofen selectively inhibits excitatory synaptic transmission in the hippocampus
Lanthorn, T. H., & Cotman, C. W. (1981) · Brain Research · doi:10.1016/0006-8993(81)90326-7 · Cited by 160 · see citing works
Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors
Colbert, C. M., & Levy, W. B. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.1.1 · Cited by 158 · see citing works
Some Networks that can Learn, Remember, and Reproduce any Number of Complicated Space‐time
Grossberg, S. (1970) · Studies in Applied Mathematics · doi:10.1002/sapm1970492135 · Cited by 156 · see citing works
Computer simulation of carbachol‐driven rhythmic population oscillations in the CA3 region of the in vitro rat hippocampus.
Traub, R. D., Miles, R., & Buzsáki, G. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019184 · Cited by 150 · see citing works
Anatomical and Functional Aspects of the Septo‐Hippocampal Projections
LYNCH, G. S., Rose, G., & Gall, C. M. (1978) · Novartis Foundation symposium · doi:10.1002/9780470720394.ch3 · Cited by 149 · see citing works
Acetylcholine potentiates responses to in the rat hippocampus
Markram, H., & Segal, M. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90495-u · Cited by 141 · see citing works
The representation and storage of information in neural networks in the primate cerebral cortex and hippocampus
Rolls, E. T. (1989) · Addison-Wesley Longman Publishing Co., Inc. eBooks · Cited by 132 · see citing works
Simple memory: a theory for archicortex
Marr, D., Willshaw, D., & McNaughton, B. (1991) · From the Retina to the Neocortex · doi:10.1007/978-1-4684-6775-8_5 · Cited by 130 · see citing works
Learning and memory is reflected in the responses of reinforcement- related neurons in the primate basal forebrain
Wilson, F., & Rolls, E. T. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01254.1990 · Cited by 120 · see citing works
Presynaptic action of acetylcholine in thin sections from the guinea pig dentate gyrus in vitro
Yamamoto, C., & Kawai, N. (1967) · Experimental Neurology · doi:10.1016/0014-4886(67)90016-7 · Cited by 118 · see citing works
Acetylcholine and Learning in a Cortical Associative Memory
Hasselmo, M. E. (1993) · Neural Computation · doi:10.1162/neco.1993.5.1.32 · Cited by 104 · see citing works
Self-citation
Fimbria-Fornix lesions impair spatial working memory but not cognitive mapping.
Walker, J. A., & Olton, D. S. (1984) · Behavioral Neuroscience · doi:10.1037/0735-7044.98.2.226 · Cited by 99 · see citing works
Intraseptal connections redefined: lack of a lateral septum to medial septum path
Léránth, C., Deller, T., & Buzsáki, G. (1992) · Brain Research · doi:10.1016/s0006-8993(10)80004-6 · Cited by 97 · see citing works
Central cholinergic involvement in working memory: Effects of scopolamine on continuous nonmatching and discrimination performance in the rat.
Spencer, D. G., Pontecorvo, M. J., & Heise, G. A. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.6.1049 · Cited by 97 · see citing works
Modulation of associative memory function in a biophysical simulation of rat piriform cortex
Barkai, E., Bergman, R. E., Horwitz, G. D., & Hasselmo, M. E. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.72.2.659 · Cited by 96 · see citing works
Self-citation
Presynaptic M1 muscarinic cholinoceptors mediate inhibition of excitatory synaptic transmission in the hippocampus in vitro
Sheridan, R. D., & Sutor, B. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90653-q · Cited by 95 · see citing works
Functions of the Septo-Hippocampal System
Hécaen, H. (1979) · Neuropsychologia · doi:10.1016/0028-3932(79)90048-4 · Cited by 85 · see citing works
γ‐Aminobutyric acid and inhibition in the septal nuclei of the rat
McLennan, H., & Miller, J. J. (1974) · The Journal of Physiology · doi:10.1113/jphysiol.1974.sp010501 · Cited by 85 · see citing works
Central cholinergic involvement in working memory: Effects of scopolamine on continuous nonmatching and discrimination performance in the rat.
Spencer, D. G., Pontecorvo, M. J., & Heise, G. A. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.6.1049 · Cited by 83 · see citing works
Perforant pathway activation of hippocampal CA1 stratum pyramidale neurons: Electrophysiological evidence for a direct pathway
Doller, H. J., & Weight, F. F. (1982) · Brain Research · doi:10.1016/0006-8993(82)90553-4 · Cited by 81 · see citing works
Runaway synaptic modification in models of cortex: Implications for Alzheimer's disease
Hasselmo, M. E. (1994) · Neural Networks · doi:10.1016/0893-6080(94)90053-1 · Cited by 80 · see citing works
Self-citation
Pharmacology of the dendritic action of acetylcholine and further observations on the somatic disinhibition in the rat hippocampusin situ
Rovira, C., Ben‐Ari, Y., CherubiniP, E., Krnjević, K., & Ropert, N. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90028-3 · Cited by 77 · see citing works
Acetylcholinesterase fiber staining in the human hippocampus and parahippocampal gyrus
Green, R. C., & Mesulam, M. M. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902730405 · Cited by 72 · see citing works
Muscarinic depression of synaptic transmission at the hippocampal mossy fiber synapse
Williams, S., & Johnston, D. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.4.1089 · Cited by 61 · see citing works
Septal lesions, intramaze cues and spatial behavior in rats
Beatty, W. W., & Carbone, C. P. (1980) · Physiology & Behavior · doi:10.1016/0031-9384(80)90395-9 · Cited by 37 · see citing works
Selective suppression of afferent but not intrinsic fiber synaptic transmission by 2-amino-4-phosphonobutyric acid (AP4) in piriform cortex
Hasselmo, M. E., & Bower, J. M. (1991) · Brain Research · doi:10.1016/0006-8993(91)91128-n · Cited by 36 · see citing works
Self-citation
Elemental Adaptive Processes of Neurons and Synapses: A Statistical/Computational Perspective
Gluck, M. A., & Rumelhart, D. E. (2013) · Psychology Press eBooks · doi:10.4324/9780203762981-10 · Cited by 36 · see citing works
Quantitative effects of some muscarinic agonists on evoked surface‐negative field potentials recorded from the guinea‐pig olfactory cortex slice
Williams, S. H., & Constanti, A. (1988) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1988.tb11471.x · Cited by 29 · see citing works
Perforant pathway-evoked long-term potentiation of CA1 neurons in the hippocampal slice preparation
Doller, H. J., & Weight, F. F. (1985) · Brain Research · doi:10.1016/0006-8993(85)91584-7 · Cited by 29 · see citing works
Presynaptic inhibitory effect of acetylcholine in the hippocampus
Dingledine, R., & Valentino, R. J. (2021) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/xfet-3138 · Cited by 18 · see citing works
Acetylcholine and Cortical Oscillatory Dynamics
Liljenström, H., & Hasselmo, M. (1993) · Springer eBooks · doi:10.1007/978-1-4615-3254-5_79 · Cited by 12 · see citing works
Self-citation
Modulation of Neuronal Adaptation and Cortical Associative Memory Function.
Hasselmo, M. E., Barkai, E., Horwitz, G. D., et al. (1994) · Springer eBooks · doi:10.1007/978-1-4615-2714-5_46 · Cited by 10 · see citing works
Self-citation
Cholinergic Modulation of Associative Memory Function in a Realistic Computational Model of Piriform Cortex
Bergman, R. E., Vanier, M. C., Horwitz, G. D., et al. (1993) · Springer eBooks · doi:10.1007/978-1-4615-3254-5_42 · Cited by 3 · see citing works

Flagged first, then by citations

Sorted by citations

Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Uncertainty, Neuromodulation, and Attention
Yu, A. J., & Dayan, P. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.026 · Cited by 1,774 · see citing works
Pyramidal neurons: dendritic structure and synaptic integration
Spruston, N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2286 · Cited by 1,688 · see citing works
Mammalian nicotinic acetylcholine receptors: from structure to function
Albuquerque, E. X., Pereira, E. F. R., Alkondon, M., & Rogers, S. W. (2009) · Physiological Reviews · doi:10.1152/physrev.00015.2008 · Cited by 1,724 · see citing works
The role of acetylcholine in learning and memory
Hasselmo, M. E. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.09.002 · Cited by 1,693 · see citing works
Self-citation
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro
Fisahn, A., Pike, F. G., Buhl, E. H., & Paulsen, O. (1998) · Nature · doi:10.1038/28179 · Cited by 884 · see citing works
Neuromodulation: acetylcholine and memory consolidation
Hasselmo, M. E. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01365-0 · Cited by 809 · see citing works
Self-citation
What Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated
Kumaran, D., Hassabis, D., & McClelland, J. L. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.05.004 · Cited by 736 · see citing works
Modes and models of forebrain cholinergic neuromodulation of cognition
Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733 · see citing works
Self-citation
Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection
Sarter, M., Hasselmo, M. E., Bruno, J. P., & Givens, B. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.08.006 · Cited by 667 · see citing works
Self-citation
Relating Hippocampal Circuitry to Function
Lisman, J. E. (1999) · Neuron · doi:10.1016/s0896-6273(00)81085-5 · Cited by 607 · see citing works
High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation
Hasselmo, M. E., & McGaughy, J. (2004) · Progress in Brain Research · doi:10.1016/s0079-6123(03)45015-2 · Cited by 525 · see citing works
Self-citation
What is the function of hippocampal theta rhythm?--Linking behavioral data to phasic properties of field potential and unit recording data
Hasselmo, M. E. (2005) · Hippocampus · doi:10.1002/hipo.20116 · Cited by 502 · see citing works
Self-citation
Novelty or Surprise?
Barto, A., Mirolli, M., & Baldassarre, G. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00907 · Cited by 397 · see citing works
“It refers to the following processes (Hasselmo and Schnell, 1994; Kumaran and Maguire, 2007; Duncan et al., 2012): (a) familiar aspects of the percept (“lures”) actively recall previous memories on the basis of pattern-completion-like mechanisms, for example, an item recalls other items previously…”
Background
Cognitive functions of the basal forebrain
Baxter, M. G., & Chiba, A. A. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80024-5 · Cited by 351 · see citing works
Place-Selective Firing of CA1 Pyramidal Cells during Sharp Wave/Ripple Network Patterns in Exploratory Behavior
O'Neill, J., Senior, T., & Csicsvari, J. (2006) · Neuron · doi:10.1016/j.neuron.2005.10.037 · Cited by 281 · see citing works
The role of hippocampal subregions in detecting spatial novelty
Lee, I., Hunsaker, M. R., & Kesner, R. P. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.145 · Cited by 270 · see citing works
The cholinergic system and hippocampal plasticity
Drever, B. D., Riedel, G., & Platt, B. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.037 · Cited by 240 · see citing works
Noradrenergic Suppression of Synaptic Transmission May Influence Cortical Signal-to-Noise Ratio
Hasselmo, M. E., Linster, C., Patil, M., Ma, D., & Cekic, M. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3326 · Cited by 229 · see citing works
Self-citation
Prediction and memory: A predictive coding account
Barron, H. C., Auksztulewicz, R., & Friston, K. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101821 · Cited by 220 · see citing works
Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: possible differential effect depending on the source of input
Kimura, F., Fukuda, M., & Tsumoto, T. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00779.x · Cited by 165 · see citing works
Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist
Hsieh, C. Y., Cruikshank, S. J., & Metherate, R. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02766-9 · Cited by 165 · see citing works
Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus
Vogt, K. E., & Regehr, W. G. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00075.2001 · Cited by 149 · see citing works
Cholinergic modulation of the hippocampus during encoding and retrieval
Rogers, J. L., & Kesner, R. P. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00063-7 · Cited by 141 · see citing works
An insula hierarchical network architecture for active interoceptive inference
Fermin, A. S. R., Friston, K., & Yamawaki, S. (2022) · Royal Society Open Science · doi:10.1098/rsos.220226 · Cited by 101 · see citing works
Dynamics of Memory Representations in Networks with Novelty-Facilitated Synaptic Plasticity
Blumenfeld, B., Preminger, S., Sagi, D., & Tsodyks, M. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.016 · Cited by 79 · see citing works
Muscarinic Activation of a Cation Current and Associated Current Noise in Entorhinal-Cortex Layer-II Neurons
Shalinsky, M. H., Magistretti, J., Ma, L., & Alonso, A. A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.3.1197 · Cited by 65 · see citing works
Nicotinic modulation of glutamatergic synaptic transmission in region CA3 of the hippocampus
Giocomo, L. M., & Hasselmo, M. E. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04316.x · Cited by 52 · see citing works
Self-citation
Perforant path activation modulates the induction of long-term potentiation of the schaffer collateral—hippocampal CA1 response: theoretical and experimental analyses
Levy, W. B., Desmond, N. L., & Zhang, D. X. (1998) · Learning & Memory · doi:10.1101/lm.4.6.510 · Cited by 43 · see citing works
Community-based reconstruction and simulation of a full-scale model of the rat hippocampus CA1 region
Romani, A., Antonietti, A., Bella, D., Budd, J., Giacalone, E., Kurban, K., Sáray, S., Abdellah, M., Arnaudon, A., Boci, E., et al. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002861 · Cited by 39 · see citing works
Evolution in Neuromodulation—The Differential Roles of Acetylcholine in Higher Order Association vs. Primary Visual Cortices
Galvin, V. C., Arnsten, A. F. T., & Wang, M. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00067 · Cited by 25 · see citing works
Cholinergic and Adenosinergic Modulation of Synaptic Release
Yang, D., Ding, C., Qi, G., & Feldmeyer, D. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2020.06.006 · Cited by 24 · see citing works
Sensory mismatch induces autonomic responses associated with hippocampal theta waves in rats
Aitake, M., Hori, E., Matsumoto, J., Umeno, K., Fukuda, M., Ono, T., & Nishijo, H. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.011 · Cited by 17 · see citing works
Rat hippocampal theta rhythm during sensory mismatch
Zou, D., Aitake, M., Hori, E., Umeno, K., Fukuda, M., Ono, T., & Nishijo, H. (2009) · Hippocampus · doi:10.1002/hipo.20524 · Cited by 17 · see citing works
Cholinergic modulation of excitatory synaptic input integration in hippocampal CA1: Acetylcholine and excitatory synaptic integration in hippocampal CA1
McQuiston, A. R. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.188581 · Cited by 16 · see citing works

Hemispheric differences in hippocampal volume predict verbal and spatial memory performance in patients with Alzheimer's disease
de Toledo‐Morrell, L., Dickerson, B. C., Sullivan, M. P. O., Spanovic, C., Wilson, R. S., & Bennett, D. A. (2000) · Hippocampus · doi:10.1002/(sici)1098-1063(2000)10:2 · Cited by 178 · see citing works
Do Interictal Discharges Promote or Control Seizures? Experimental Evidence from an In Vitro Model of Epileptiform Discharge
Avoli, M. (2001) · Epilepsia · doi:10.1046/j.1528-1157.2001.042suppl.3002.x · Cited by 84 · see citing works
Anatomical and Physiological Properties of GABAergic Neurotransmission in Organotypic Slice Cultures of Rat Hippocampus
Streit, P., Thompson, S. M., & Gähwiler, B. H. (1989) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1989.tb00366.x · Cited by 66 · see citing works
Neurohumoral Mechanisms in the Brain Slice
Katz, R. I., & Chase, T. N. (1971) · Advances in pharmacology · doi:10.1016/s1054-3589(08)60592-x · Cited by 24 · see citing works
Synaptic GABAergic transmission in the central amygdala (CeA) of rats depends on slice preparation and recording conditions
Avegno, E. M., Middleton, J. W., & Gilpin, N. W. (2019) · Physiological Reports · doi:10.14814/phy2.14245 · Cited by 7 · see citing works

Authors: Hasselmo, M., & Schnell, E.
Affiliations: Harvard University (US)
ORCID: Schnell, E
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 1994-06-01
Volume: 14
Issue: 6
Pages: 3898-3914
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.14-06-03898.1994
PMC: PMC6576918
OpenAlex: W2161627797
Cited by: 466
References: 83
Citations by year: 2026: 9 · 2025: 16 · 2024: 9 · 2023: 11 · 2022: 11 · 2021: 11 · 2020: 14 · 2019: 13 · 2018: 18 · 2017: 16 · 2016: 14 · 2015: 9 · 2014: 11 · 2013: 10 · 2012: 19
FWCI: 8.80
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 183 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Office of Naval Research
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: cholinergic modulation, acetylcholine, hippocampal CA1, Schaffer collateral synapses, stratum radiatum, stratum lacunosum-moleculare, synaptic transmission, carbachol, muscarinic receptors, atropine, associative memory, computational model
MeSH terms: Animals, Association Learning, Atropine, Bicuculline, Brain, Carbachol, Feedback, Female, Hippocampus, Models, Neurological, Synaptic Transmission, Parasympathomimetics, Mental Recall, Rats, Sprague-Dawley, Rats

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.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks