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Modulation of Synaptic Responses in the Entorhinal Cortex Evoked by Repetitive Stimulation of the Parasubiculum

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Modulation of Synaptic Responses in the Entorhinal Cortex Evoked by Repetitive Stimulation of the Parasubiculum

Sparks, Daniel W (2016) Modulation of Synaptic Responses in the Entorhinal Cortex Evoked by Repetitive Stimulation of the Parasubiculum. PhD thesis, Concordia University.

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Abstract

The entorhinal cortex provides the hippocampus with the majority of its sensory input. The entorhinal cortex also receives the largest output projection of the parasubiculum, a structure that receives output projections from the hippocampus. The parasubicular projection to the entorhinal cortex could play a critical role in determining how the entorhinal cortex responds to incoming sensory inputs. Therefore, alterations in how the entorhinal cortex responds to and processes sensory input, influenced by its projection from the parasubiculum, could be important for mnemonic processing the hippocampus. Neural activity in brain regions throughout the hippocampal formation, including the parasubiculum and entorhinal cortex, is heavily modulated by the neurotransmitter acetylcholine and the associated theta- and gamma-frequency oscillatory EEG rhythms. However, it is not known how cholinergic activity and synaptic inputs at these frequencies affect communication between the parasubiculum and entorhinal cortex, and how this could influence the processing of sensory inputs within the entorhinal cortex.
The first experiments in this thesis utilized field potential recordings of excitatory postsynaptic potentials (fEPSPs), and found that activation of cholinergic receptors, despite reducing the amplitude of responses to single pulses of stimulation, facilitated entorhinal cortex responses during trains of stimulation of the parasubiculum at both theta- and gamma- frequencies. This effect was found to be reliant upon M1 muscarinic receptors and was associated with cholinergic reductions in the cationic conductance Ih. In a second series of experiments, intracellular recordings of EPSPs in stellate cells in layer II of the medial entorhinal cortex replicated the findings obtained in field potential recordings, and indicated that the facilitation of train-evoked responses at theta- and gamma-frequencies by cholinergic agonism is due in part to reductions in Ih that lead to increased input resistance and widening of EPSPs. In a third series of experiments, when a second stimulating electrode was placed in layer I of the medial entorhinal cortex to activate sensory input pathways, it was found that trains of stimulation in the
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parasubiculum at theta-frequency modulated the strength of subsequent entorhinal cortex responses to incoming layer I sensory inputs. Stimulation of the parasubiculum was found to either suppress or facilitate responses to layer I inputs depending on the interval between parasubicular and layer I stimulation, suggesting that the parasubiculum can influence the ongoing processing of sensory inputs by the entorhinal cortex. When prolonged, repetitive, delivery of theta-frequency parasubicular stimulation trains was paired with single pulses of stimulation of layer I at short intervals after each train, it was found that co-activation of these inputs pathways resulted in a selective and lasting depression of entorhinal cortex responses to layer I stimulation. These results indicate that activation of the parasubiculum can have a lasting impact on how the entorhinal cortex responds to sensory inputs. Overall these results have strong implications for how information is processed in the hippocampal formation, and suggest that parasubicular inputs to the entorhinal cortex can influence the nature of the sensory and associational information that the entorhinal cortex provides to the hippocampus.

Divisions:Concordia University > Faculty of Arts and Science > Psychology
Concordia University > Research Units > Centre for Studies in Behavioural Neurobiology
Item Type:Thesis (PhD)
Authors:Sparks, Daniel W
Institution:Concordia University
Degree Name:Ph. D.
Program:Psychology
Date:22 June 2016
Thesis Supervisor(s):Chapman, C. Andrew
ID Code:981339
Deposited By: DANIEL SPARKS
Deposited On:09 Nov 2016 20:21
Last Modified:18 Jan 2018 17:52

References:

REFERENCES
Abrahamsson T, Cathala L, Matsui K, Shigemoto R, DiGregorio DA (2012) Thin dendrites of cerebellar interneurons confer sublinear synaptic integration and a gradient of short-term plasticity. Neuron 73:1159-1172.
Adams JP, Dudek SM (2005) Late-phase long-term potentiation: Getting to the nucleus. Nat Rev Neurosci 6:737-743.
Alonso A, deCurtis M, Llinas R (1990) Postsynanptic hebbian and non-hebbian long-term potentiation of synaptic efficacy in the entorhinal cortex in slices and in the isolated adult guinea pig brain. P Natl Acad Sci USA 87:9280-9284.
Alonso A, Klink R (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70:128-143.
Alonso A, Kohler C (1984) A study of the reciprocal connections between the septum and the entorhinal area using anterograde and retrograde axonal transport methods in the rat brain. J Comp Neurol 225:327-343.
Amaral DG (1993) Emerging principles of intrinsic hippocampal organization. Curr Opin Neurobiol 3:225-229.
Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 31:571-591.
Andersen P, Bland BH, Dudar JD (1973) Organization of the hippocampal output. Exp Brain Res 17:152-168.
Andersen P, Holmqvist B, Voorhoeve PE (1966b) Excitatory synapses on hippocampal apical dendrites activated by entorhinal stimulation. Acta Physiol Scand 66:461-472.
Arai A, Lynch G (1992) Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation. Brain Res 598:173–184.
Aramakis VB, Bandrowski AE, Ashe JH (1999) Role of muscarinic receptors, G-proteins, and intracellular messengers in muscarinic modulation of NMDA receptor-mediated synaptic transmission. Synapse 32:262–275.
Artola A, von Frijtag JC, Fermont PCJ, Gispen WH, Scharma LH, Kamal A, Spruijt BM (2006) Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci 23:261-272.
134
Atherton JF, Kitano K, Baufreton J, Fan K, Wokosin D, Tkatch T, Shigemoto R, Surmeier DJ, Bevan MD (2010) Selective participation of somatodendritic HCN channels in inhibitory but not excitatory synaptic integration in neurons of the subthalamic nucleus. J Neurosci 30:16025–16040.
Auerbach JM, Segal M (1996) Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492:479-493.
Barrett SG, Chapman CA (2013) Contribution of muscarinic M1 receptors to the cholinergic suppression of synaptic responses in layer II of the entorhinal cortex. Neuroscience 554:11-15.
Barry C, Bush D (2012) From A to Z: A potential role for grid cells in spatial navigation. Neural Systems & Circuits 2:1-8.
Barry C, Heys JG, Hasselmo ME (2012) Possible roles of Acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells. Front Neural Circuits 6:1–13.
Basar E, Basar-Eroglu C, Karakas S, Schurmann M (2000) Brain oscillations in perception and memory. Int J Psychophysiol 35:95-124.
Belluscio MA, Mizuseki K, Schmidt R, Kempter R, Buzsaki G (2012) Cross-frequency phase- phase coupling between theta and gamma oscillations in the hippocampus. J Neurosci 32:423-435.
Bender RA, Brewster A, Santoro B, Ludwig A, Hofmann F, Biel M, Baram TZ (2001) Differential and age-dependent expression of hyperpolarization-activated cyclic nucleotide-gated cationchannel isoforms 1-4 suggests evolving roles in the developing rat hippocampus. Neuroscience 106:689-698.
Bently P, Driver J, Dolan RJ (2011) Cholinergic modulation of cognition: Insights from human pharmacological functional neuroimaging. Prog Neurobio 94:360-388.
Berretta N, Jones RSG (1996) Tonic facilitation of glutamate release by presynaptic N-methyl-D- aspartate autoreceptors in the entorhinal cortex. Neuroscience 75:339-344.
Birtoli B, Ulrich D (2004) Firing mode-dependent synaptic plasticity in rat neocortical pyramidal neurons. J Neurosci 24:4935-4940.
Bizenhofer SH, Sieben, K, Siebert KD, Spehr M, Hanganu-Opatz IL (2015) Oscillatory activity in developing prefrontal networks results from theta-gamma-modulated synaptic inputs. Cell Rep 11:486-497.
135
Blackstad TW (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105:417-537.
Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331- 356.
Blokland A (1996) Acetylcholine: A neurotransmitter for learning and memory? Brain Res Rev 21:285-300.
Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser MB (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987-994.
Bouras R, Chapman CA (2003) Long-term synaptic depression in the adult entorhinal cortex in vivo. Hippocampus 13:780–790.
Brazhnik ES, Muller RU, Fox SE (2003) Muscarinic blockade slows and degrades the location- specific firing of hippocampal pyramidal cells. J Neurosci 23:611–621.
Brazhnik ES, Ramie B, Muller RU, Fox SE (2004) The effects on place cells of local scopolamine dialysis are mimicked by a mixture of two specific muscarinic antagonists. J Neurosci 24:9313–9323.
Brenowitz S, Trussel LO (2001) Minimizing synaptic depression by control of release probability. J Neurosci 21:1857–1867.
Brun VH, Otnaess MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243-2246.
Burwell RD (2000) The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci 911:25-42.
Burwell RD, Amaral DG (1998) Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex. Journal Comp Neurol 391:293-321.
Burwell RD, Witter MP, Amaral DG (1995) Perirhinal and postrhinal cortices of the rat: a review of neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5:390–408.
Bush PC, Sejnowski TJ (1994) Effects of inhibition and dendritic saturation in simulated neocortical pyramidal cells. J Neurophysiol 71:2183-2193.
Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.
136
Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science, 304:1926- 1929.
Buzsaki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal- entorhinal system. Nat Neurosci 16:130-138.
Buzsaki G, Watson BO (2012) Brain rhythms and neural syntax: Implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin Neurosci 14:345-367.
Bzelot M, Bocchio M, Kasugai Y, Fischer D, Dodson PD, Ferraguti F, Capogna M (2015) Hippocampal theta input to the amygdala shapes feedforward inhibition to gate heterosynaptic plasticity. Neuron 87:1290-1303.
Caballero-Bleda M, Witter MP (1993) Regional and laminar organization of projections from the presubiculum and parasubiculum to the entorhinal cortex: an anterograde tracing study in the rat. J Comp Neurol 328:115-129.
Caballero-Bleda M, Witter M.P (1994) Projections from the presubiculum and the parasubiculum to morphologically characterized entorhinal-hippocampal projection neurons in the rat. Exp Brain Res 101:93-108.
Cacucci F, Lever C, Wills TJ, Burgess N, O’Keefe J (2004) Theta- modulated place-by-direction cells in the hippocampal formation in the rat. J Neurosci 24:8265–8277.
Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14:506-515.
Canto CB, Koganezawa N, Breed P, Moser EI, Witter MP (2012) All layers of medial entorhinal cortex receive presubicular and parasubicular inputs. J Neurosci 32:17620-17631.
Canto CB, Witter MP (2012) Cellular properties of principal neurons in the rat entorhinal cortex.
II. The medial entorhinal cortex. Hippocampus 22:1277-1299.
Canto CB, Wouterlood FG, Witter MP (2008). What does the anatomical organization of the
entorhinal cortex tell us? Neural Plast 2008:1-18.
Carr DB, Andrews GD, William BG, Lavin A (2007) a2-Noradrenergic receptors activation
enhances excitability and synaptic integration in rat prefrontal cortex pyramidal neurons via inhibition of HCN currents. J physiol 584:437–450.
137

Carr DB, Surmeier DJ (2007) M1 muscarinic receptor modulation of Kir2 channels enhances temporal summation of excitatory synaptic potentials in prefrontal cortex pyramidal neurons. J Neurophysiol 97:3432-3438.
Caruana DA, Chapman CA (2004). Stimulation of the parasubiculum modulates entorhinal cortex responses to piriform cortex inputs in vivo. J Neurophysiol 92:1226-1235.
Castro-Alamancos MA, Connors BW (1996) Cellular mechanisms of the augmenting response: short-term plasticity in a thalamacortical pathway. J Neurosci 16:7742–7756.
Caulfield MP, Birdsall NJM (1998) International union of pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Am Soc Pharmacol Exp Ther 50:279–290.
Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56:1-26. Chapman CA, Lacaille JC (1999) Cholinergic induction of theta- frequency oscillations in
hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J Neurosci
19:8637–8645.
Chapman CA, Racine RJ (1997) Converging inputs to the entorhinal cortex from the piriform
cortex and medial septum: Facilitation and current source density analysis. J
Neurophysiol 78:2602–2615.
Cheong MI, Yun SH, Mook-Jung I, Joo I, Huh K. Jung MW (2001) Cholinergic modulation of
synaptic physiology in deep layer entorhinal cortex of the rat. J Neurosci Res 66:117-121. Chevaleyre V, Castillo PE (2002) Assessing the role of Ih channels in synaptic transmission and
mossy fiber LTP. PNAS 99:9538–9543.
Chistiakova M, Bannon NM, Bazhenov M, Volgushev M (2014) Heterosynaptic plasticity:
Multiple mechanisms and multiple roles. Neuroscientist 20:483-498.
Chistiakova M, Volgushev M (2009) Heterosynaptic plasticity in the neocortex. Exp Brain Res
199:377-390.
Cho YH, Kesner RP (1996) Involvement of entorhinal cortex or parietal cortex in long-term
discrimination memory in rats: Retrograde amnesia. Behav Neurosci 110:436-442. Chrobak JJ, Buzsaki G (1998) gamma oscillations in the entorhinal cortex of the freely behaving
rat. J Neurosci 18: 388-398.
Colgin LL (2011) Oscillations and hippocampal-prefrontal synchrony. Curr Opin Neurobiol
21:467-474.
138
Colgin LL (2013) Mechanisms and functions of theta rhythms. Annu Rev Neurosci 36:295-312. Colgin LL (2015) Theta-gamma coupling in the entorhinal-hippocampal system. Curr Opin
Neurobiol 31:45-50.
Colgin LL, Denniger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009)
Frequency of gamma oscillations routes flow of information in the hippocampus. Nature
462: 353-358.
Craig MT, McBain CJ (2015) Navigating the circuitry of the brain’s GPS system: Future
challenges for neurophysiologists. Hippocampus 25:736-743.
Dasari S, Gulledge AT (2011) M1 and M4 receptors modulate hippocampal pyramidal neurons. J
Neurophysiol 105:779-792.
Davies CH, Collingridge GL (1996) Regulation of EPSPs by the synaptic activation of GABAB
autoreceptors in rat hippocampus. J Physiol 496:451–470.
Day M, Carr DB, Ulrich S, Ilijic E, Tkatch T, Surmeier DJ (2005) Dendritic excitability of
mouse frontal cortex pyramidal neurons is shaped by the interaction among HCN, Kir2,
and Kleak channels. J Neurosci 25:8776-8787.
Deng PY, Lei S. (2007) Long-term depression in identified stellate neurons of juvenile rat
entorhinal cortex. J Neurophysiol, 97:727-737.
de Curtis M, Pare D (2004) The rhinal cortices: a wall of inhibition between the neocortex and
the hippocampus. Prog Neurobiol 74:101–110.
Deisz RA, Prince DA (1989) Frequency-dependent depression of inhibition in guinea-pig
neocortex in vitro by GABAB receptor feed-back on GABA release. J Physiol 412:513-
541.
Dickson CT, Biella G, de Curtis M (2000a) Evidence for spatial modules mediated by temporal
synchronization of carbachol-induced gamma rhythm in medial entorhinal cortex. J
Neurosci 20:7846-7854.
Dickson CT, de Curtis M (2002) Enhancement of temporal and spatial synchronization of
entorhinal gamma activity by phase reset. Hippocampus 12:447–456.
Dickson CT, Magistretti J, Shalinsky MH, Fransen E, Hasselmo ME, Alonso A (2000b)
Properties and role of Ih in pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J Neurophys 83:2562-2579.
139
Douchamps V, Jeewajee A, Blundell P, Burgess N, Lever C. (2013) Evidence for encoding versus retrieval scheduling in the hippocampus by theta phase and acetylcholine. J Neurosci, 33:8689-8704.
Douglas RJ (1967). The hippocampus and behavior. Psychol Bull 67:416-422.
Doyere V, Errington ML, Laroche S, Bliss TVP (1996) Low-frequency trains of paired stimuli
induce long-term depression in area CA1 but not dentate gyrus of the intact rat.
Hippocampus 6:52-57.
Drever BD, Riedel G, Platt R. (2011) The cholinergic system and hippocampal plasticity. Behav
Brain Res 221:505-514.
Dutar P, Nicoll RA (1988) Classification of muscarinic responses in hippocampus in terms of
receptor subtypes and second-messenger systems: Electrophysiological studies in vitro. J
Neurosci 8:4214-4224.
Duzel E, Penny WD, Burgess N (2010) Brain oscillations and memory. Curr Opin Neurobiol
20:143-149.
Easton A, Douchamps V, Eacott M, Lever C (2013) A specific role for septohippocampal
acetylcholine in memory? Neuropsychologica 50:3156-3168.
Economo MN, Martínez JJ, White JA (2014) Membrane potential-dependent integration of
synaptic inputs in entorhinal stellate neurons. Hippocampus 24:1493-505. Eichenbaum H, Sauvage M, Fortin N, Komorowski R, Lipton P (2012) Towards a functional
organization of episodic memory in the medial temporal lobe. Neurosci Biobehav Rev
36:1597–1608.
Feldman DE (2012) The spike timing dependence of plasticity. Neuron 75: 556-571. Fernandez FR, Malebra P, Bressloff PC, White JA (2013) Entorhinal stellate cells show
preferred spike phase-locking to theta inputs that is enhanced by correlations in synaptic
activity. J Neurosc 33:6027-6040.
Fiashn A, Yamada M, Duttaroy A, Gan JW, Deng CX, McBain CJ, Wess J (2002) Muscarinic
induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two
mixed cation currents. Neuron 33:615-624.
Forster E, Zhao S, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7:259-
267.
140
Funahashi M, Stewart M (1997a) Presubicular and parasubicular cortical neurons of the rat: electrophysiological and morphological properties. Hippocampus 7:117-129. Funahashi M, Stewart M (1997b) Presubicular and parasubicular cortical neurons of the rat:
functional separation of deep and superficial neurons in vitro. J Physiol 501:387-403. Funahashi M, Stewart M (1998) GABA receptor-mediated post- synaptic potentials in the
retrohippocampal cortices: regional, laminar and cellular comparisons. Brain Res
787:19–33.
Furtak SC, Wei SM, Agster KL, Burweel RD (2007) Functional neuroanatomy of the
parahippocampal region in the rat: The perirhinal and postrhinal cortices. Hippocampus
17:709-722.
Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the
entorhinal cortex. Science 305:1258-1264.
Garden DLF, Dodson PD, O’Donnel C, White MD, Nolan MF (2008) Tuning of synaptic
integration in the medial entorhinal cortex to the organization of grid cell firing fields.
Neuron 60:875–889.
Gaykema RPA, Luiten PGM, Nyakas C, Traber J (1990) Cortical projection patterns of the
medial septum–diagonal band complex. J Comp Neurol 293:103–124.
George MS, Abbott LF, Siegelbaum SA (2009) HCN hyperpolarization-activated cation
channels inhibit EPSPs by interactions with M-type K+ channels. Nat Neurosci 12:577-
584.
Giocomo LM, Zilli EA, Fransen E, Hasselmo ME (2007) Temporal frequency of subthreshold
oscillations scales with entorhinal grid cell field spacing. Science 315:1719–1722. Glasgow SD, Chapman CA (2007) Local generation of theta-frequency EEG activity in the
parasubiculum. J Neurophysiol 97:3868-3879.
Glasgow SD, Chapman CA (2008) Conductances mediating intrinsic theta-frequency membrane
potential oscillations in layer II parasubicular neurons. J Neurophysiol 100:2746-2756. Glasgow SD, Chapman CA (2013) Muscarinic depolarization of layer II neurons of the
parasubiculum. PLoS One, 8, 1-14.
Glasgow SD, Glovaci I, Karpowicz LS, Chapman CA (2012) Cholinergic suppression of
excitatory synaptic transmission in layers II/III of the parasubiculum. Neuroscience 201:1-11.
141
Gloveli T, Egorov AV, Schmitz D, Heinemann U, Muller W (1999) Carbachol-induced changes in excitability and [Ca2+]i signaling in projection cells of medial entorhinal cortex layers II and III. Eur J Neurosci 11:3626–3636.
Good M (2002) Spatial memory and hippocampal function: Where are we now? Psicologica 23:109-138.
Grover LM, Kim E, Cooke JD, Holmes WR (2009) LTP in hippocampal area CA1 is induced by burst stimulation over a broad frequency range centered around delta. Learn Mem 16:69- 81.
Grover LM, Yan C (1999) Blockade of GABAA receptors facilitates induction of NMDA receptor-independent long-term potentiation. J Neurophysiol 81:2814-2822.
Haas JS, White JA (2002) Frequency selectivity of layer II stellate cells in medial entorhinal cortex. J Neurophysiol 88:2422–2429.
Habib D, Tsui CKY, Rosen LG, Dringenberg HC (2013) Occlusion of low-frequency-induced, heterosynaptic long-term potentiation in the rat hippocampus in vivo following spatial training. Cereb Cortex 24:3090-3096.
Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI (2008) Hippocampus-independent phase procession in entorhinal grid cells. Nature Lett 453:1248-1253.
Hamam BN, Sinai M, Poirier G, Chapman CA (2007) Cholinergic suppression of excitatory synaptic responses in layer II of the medial entorhinal cortex. Hippocampus 17:103-113.
Han EB, Heinemann SF (2013) Distal dendritic inputs control neuronal activity by heterosynaptic potentiation of proximal inputs. J Neurosci 33:1314-1325.
Hargreaves EL, Yoganarasimha D, Knierim JJ (2007) Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorhinal cortex, and hippocampus. Hippocampus 1: 826-841.
Hasselmo ME (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobio 16: 710-715.
Hasselmo ME (2008) Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18:1213–1229.
Hasselmo ME, Brandon MP (2012) A model combining oscillations and attractor dynamics for generation of grid cell firing. Front Neural Circuits 6:1–13.
142
Hasselmo ME, Giocomo LM, Zilli EA (2007) Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17:1252–1271.
Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (2002) Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 15:689-707.
Hasselmo ME, Sarter M (2011) Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropyschopharmacology 36:52-73.
Hasselmo ME, Stern CE (2014) Theta rhythm and the encoding and retrieval of space and time. Neuroimage 85:656-666.
Hebb DO (1949) The Organization of Behavior. New York: Wiley & Sons.
Heys JG, Giocomo LM, Hasselmo ME (2010) Cholinergic modulation of the resonance
properties of stellate cells in layer II of medial entorhinal cortex. J Neurophysiol
104:258-270.
Heys JG, Schultheiss NW, Shay CF, Tsuno Y, Hasselmo ME (2012) Effects of acetylcholine on
neuronal properties in entorhinal cortex. Front Behav Neurosci 6:1-19.
Hioki H, Okamoto S, Konno M, Kameda H, Sohn J, Kuramoto E, Fujiyama F, Kaneko T (2013)
Cell type-specific inhibitory inputs to dendritic and somatic compartments of
parvalbumin-expressing neocortical interneuron. J Neurosci 33:544-555.
Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal
propogation in dendrites of hippocampal pyramidal neurons. Nature 387:869-875. Hoffman DA, Sprengel R, Sakmann B (2002) Molecular dissection of hippocampal theta-burst
pairing potentiation. PNAS 99:7740-7745.
Hsieh LT, Ranganath C (2013) Frontal midline theta oscillations during working memory
maintenance and episodic encoding and retrieval. Neuroimage 85:721-729.
Hu H, Martina M, Jonas P (2010) Dendritic mechanisms underlying rapid synaptic activation of
fast-spiking hippocampal interneurons. Science 327:52-58.
Huang YY, Pittenger C, Kandel ER (2004) A form of long-lasting, learning-related synaptic
plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. PNAS, 101:859-864.
143
Huang Z, Lujan R, Kadurin I, Uebele VN, Renger JJ, Dolphin AC, Shah MM (2011) Presynaptic HCN1 channels regulate Cav3.2 activity and neurotransmission at select cortical synapses. Nat Neurosci 14:478–486.
Hulme SR, Jones OD, Raymond CR, Sah P, Abraham WC (2013) Mechanisms of heterosynaptic metaplasticity. Phil Trans Royal Soc B. 369:1-8.
Igarashi KM, Lu L, Colgin LL, Moser MB, Moser EI (2014) Coordination of entorhinal- hippocampal ensemble activity during associative learning. Nature: 510:143-147.
Ino T, Kaneko T, Mizuno N (2001) Projections from the hippocampal and parahippocampa; regions to the entorhinal cortex. An anterograde and retrograde tract-tracing study in the cat. Neuroscience Research 39:51-69.
Insausti R, Trinidad Herroero M, Witter MP (1997) Entorhinal cortex of the rat: Cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7:146-183.
Ito M, Kano M (1992) Long-lasting depression of parallel fiber-Purkinje cell transmission by conjunctive stimulation of parallel fibers and climing fibers in the cerebellar cortex. Neurosci Lett 33:253-258.
Jerusalinsky D, Kornisiuk E, Izquierdo I (1997) Cholinergic neurotransmission and synaptic plasticity concerning memory processing. Neurochem Res 22:507-515.
Jarrard LE, Davidson TL, Bowring B (2004) Functional differentiation within the medial temporal lobe in the rat. Hippocampus 14:434-449.
Jezek K, Henriksen EJ, Treves A, Moser EI, Moser MB (2011). Theta-paced flickering between place-cell maps in the hippocampus. Nature 478:246-251.
Johnston D, Christie BR, Frick A, Gray R, Hoffman DA, Schexnayder LK, Watanabe S, Yuan LL (2003) Active dendrites, potassium channels and synaptic plasticity. Phil Trans R Soc Lond B 358:667-674.
Jones RSG (1990) Synaptic responses of neurons in layer II of the rat medial entorhinal cortex to stimulation of the para-subiculum in vitro. Proc Physiol Soc 426:48P.
Jones RSG, Buhl EH (1993) Basket-like interneurons in layer II of the entorhinal cortex exhibit a powerful NMDA-mediated synaptic excitation. Neurosci Lett 149:35-39.
144
Judge SJ, Hasselmo ME (2004) theta rhythmic stimulation of stratum lacunosum-moleculare in rat hippocampus contributes to associative LTP at a phase offset in stratum radiatum. J Neurophysiol 92:1615-1624.
Kawasaki H, Palmieri C, Avoli M (1999) Muscarinic receptor activation induces depolarizing plateau potentials in bursting neurons of the rat subiculum. J Neurophysiol 82:2590-2601.
Kerr KM, Agster KL, Furtak SC, Burwell RD (2007) Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus 17:697- 708.
Kesner R. (1973) A neural system analysis of memory storage and retrieval. Psychol Bull 80:177-203.
Kesner RP, Giles R (1998) Neural circuit analysis of spatial working memory: Role of pre- and parasubiculum, medial and lateral entorhinal cortex. Hippocampus 8:416-423.
Khakpai F, Nasehi M, Haeri-Rohani A, Eidi A, Zarrindast MR (2013) Septo-hippocampal-septal loop and memory formation. Basic Clin Neurosc 4:5-23.
Khateb A, Fort P, Williams S, Serafin M, Jones BE, Muhlethaler M (1997) Modulation of cholinergic nucleus basalis neurons by acetylcholine and N-methyl-D-aspartate. Neuroscience 8:47–55.
Kitamura T, Pignatelli M, Suh J, Kohara K, Yoshiki A, Kuniya A, Tonegawa S (2014) Island cells control temporal association memory. Science 343:896-901.
Klink R, Alonso A (1993) Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J Neurophysiol 70:144-157.
Klink R, Alonso A (1997a) Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol 77:1829-1843.
Klink R, Alonso A (1997b) Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J Neurophysiol 77:1813-1828.
Knierim JJ (2015) From the GPS to HM: Place cells, grid cells, and memory. Hippocampus 25:719-725.
Knierim JJ, Lee I, Hargreaves EL (2006) Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 16:755– 764.
145
Knierim JJ, Neunuebel JP, Deshmukh SS (2013) Functional correlates of the lateral and medial entorhinal cortex: Objects, path integration and local-global references frames. Phil Trans Roy Roc Bio 369:20130369
Kohler C (1985) Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 236:504-522.
Kohler C (1986) Intrinsic connections of the retrohippocampal region in the rat brain. II. The medial entorhinal area. J Comp Neurol 246:149-169.
Kourrich S, Chapman CA (2003) NMDA receptor-dependent long-term synaptic depression in the entorhinal cortex in vitro. J Neurophysiol 89:2112-2119.
Kourrich S, Glasgow SD, Caruana DA, Chapman CA (2008) Postsynaptic signals mediating induction of long-term synaptic depression in the entorhinal cortex. Neural Plast 2008:1- 9.
Kremin T, Gerber D, Giocomo LM, Huang SY, Tonegawa S, Hasselmo ME (2006) Muscarinic suppression in stratum radiatum of CA1 shows dependence on presynaptic M1 receptors and is not dependent on effects at GABAB receptors. Neurobiol Learn Mem 85:153–163.
Kunitake A, Kunitake T, Stewart M (2004) Differential modulation by carbachol of four separate excitatory afferent systems to the rat subiculum in vitro. Hippocampus 14:986-999.
Larson J, Munkacsy E (2014) Theta-burst LTP. Brain Res 1621:38-50
Lasztoczi B, Klausberger T (2014) Layer-specific GABAergic control of distinct gamma
oscillations in the CA1 hippocampus. Neuron 81:1126-1139.
Lingenhohl K, Finch DM (1991) Morphological characterization of rat entorhinal neurons in
vivo: Soma-dendritic structure and axonal domains. Exp Brain Res 84:57-74. Levy WB, Steward O (1983) Temporal contiguity requirements for long-term associative
potentiation/depression in the hippocampus. Neuroscience 8:791-797.
Lisman JE, Grace AA (2005) The hippocampal-VTA loop: Controlling the entry of information
into long-term memory. Neuron 46:703-713.
Lisman JE, Jensen O (2013) The theta-gamma neural code. Neuron 77:1002-1016.
Liu P, Jarrard LE, Bilkey DK (2001) Excitotoxic lesions of the pre- and parasubiculum disrupt
object recognition and spatial memory processes. Behav Neurosci 115:112-124.
Liu P, Jarrard LE, Bilkey DK (2004) Excitotoxic lesions of the pre- and parasubiculum disrupt
the place fields of hippocampal pyramidal cells. Hippocampus 14:107-116.
146
Liu S, Shipley MT (2008) Intrinsic conductances actively shape excitatory and inhibitory postsynaptic responses in olfactory bulb external tufted cells. J Neurosci 28:10311– 10322.
Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AHM (1990) Anatomic organization of physiology of the limbic cortex. Physiol Rev 70:453-511.
Luthi A, McCormick DA (1998) H-current: Properties of a neuronal and network pacemaker. Neuron 21:9-12.
Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
Magee JC (1999) Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:508-514.
Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1:181- 190.
Magee JC (2001) Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J Neurophysiol 86:528-532.
Magistretti J, Ragsdale DS, Alonso A (1999) Direct demonstration of persistent Na+ channel activity in dendritic processes of mammalian cortical neurones. J Physiol 521:629-636.
Malenka RC, Bear MF (2004) LTP and LTD: An embarrassment of riches. Neuron 44:5-21. Malenka RC, Nicoll RA (1993) NMDA-receptor-dependent synaptic plasticity: Multiple forms
and mechanisms. TINS 16:521-527.
Markram H, Lubke J, Fortscher M, Sakmann B (1997) Regulation of synaptic efficacy by
coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA (1996). Impaired hippocampal
representation of space in CA1-specific NMDAR1 knockout mice. Cell 87:1339-1349. McQuiston AR (2010) Cholinergic modulation of excitatory synaptic input integration in
hippocampal CA1. J Physiol 588:3727-3742.
Medinilla V, Johnson O, Gasparini S (2013) Features of proximal and distal excitatory synaptic
inputs to layer V neurons of the rat medial entorhinal cortex. J Physiol 591:169-183. Metherate R, Ashe JH (1994) Facilitation of an NMDA receptor-mediated EPSP by paired-pulse stimulation in rat neocortex via depression of GABAergic IPSPs. J Physiol 481:331-348.
147
Meuth SG, Kanyshkova T, Meuth P, Landgraf P, Munsch T, Ludwig A, Hofmann F, Pape H, Budde T (2006) Membrane resting potential of thalamocortical relay neurons is shaped by the interaction among TASK3 and HCN2 channels. J Neurophys 96:1517–1529.
Mitchell SJ, Ranck JB (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res 189:49-66.
Mitchell SJ, Rawlins JNP, Steward O, Olton DS (1982) Medial septal area lesions disrupt Θ rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J Neurosci 2:292-302.
Monteggia LM, Eisch AJ, Tang MD, Kaczmarek LK, Nestler EJ (2000). Cloning and localization of the hyperpolarization-activated cyclic nueclotide-gated channel family in rat brain. Molec Brain Res 81:129-139.
Morris NP, Fyffe REW, Robertson B (2004) Characterisation of hyperpolarization-activated current (Ih) in the medial septum/diagonal band complex in the mouse. Brain Res 1006:74-86.
Morris RGM, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776.
Morris RGM, Garrud P, Rawlins JNP, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31:69-89.
Moser MB, Rowland DC, Moser EI (2015) Place cells, grid cells, and memory. Cold Spring Harb Perspect Biol 7:1-15.
Mouly AM, Di Scala G (2006) Entorhinal cortex stimulation modulates amygdala and piriform cortex responses to olfactory bulb inputs in the rat. Neuroscience 137:1131-1141.
Naber PA, Witter MP, Lopez da Silva FH (1999) Perirhinal cortex input to the hippocampus in the rat: Evidence for parallel pathways, both direct and indirect. A combined physiological and anatomical study. Eur J Neurosci 11:4119-4133.
Naber PA, Witter MP, Lopes da Silva FH (2001) Evidence for a direct projection from the postrhinal cortex to the subiculum in the rat. Hippocampus 11:105-117.
148
Nevian T, Sakmann B (2004) Single spine Ca2+ signals evoked by coincident EPSPs and backpropogating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory cortex. J Neurosci 24:1689-1699.
Newman EL, Gillet SN, Climer JR, Hasselmo ME (2013) Cholinergic blockade reduces theta- gamma phase amplitude coupling and speed modulation of theta frequency consistent with behavioral effects of encoding. J Neurosci 33:19635-19646.
Nolan MF, Dudman JT, Dodson PD, Santoro B (2007) HCN1 channels control resting and active integrative properties of stellate cells from layer II of the entorhinal cortex. J Neurosci 27:12440-12451.
Nyhus E, Curran T (2010) Functional role of gamma and theta oscillations in episodic memory. Neurosci Biobehav Rev 34:1023-1035.
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, London.
O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330.
O’Reilly KC, Alarcon JM, Ferbinteanu J (2014) Relative contributions of CA3 and medial entorhinal cortex to memory in rats. Front Behav Neurosci 8:1-17.
Palmer LM, Stuart GJ (2009) Membrane potential changes in dendritic spines during action potentials and synaptic input. J Neurosci 29:6897–6903.
Parron C, Poucet B, Save E (2006). Cooperation between the hippocampus and the entorhinal cortex in spatial memory: A disconnection study. Behav Brain Res 170:99-109.
Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. 4th ed. San Diego: Academic Press Inc.
Penley SC, Hinman JR, Sabolek HR, Escabi MA, Markus EJ, Chrobak JJ (2012) Theta and gamma coherence across the septotemporal axis during distinct behavioral states. Hippocampus 22:1164-1175.
Pepeu G, Giovannini MG (2004) Changes in acetylcholine extracellular levels during cognitive processes. Learn Mem 11:21-27.
Pian P, Bucchi A, DeCostanzo A, Robinson RB, Siegelbaum SA (2007) Modulation of cyclic nucleotide-regulated HCN channels by PIP2 and receptors coupled to phospholipase C. Eur J Physiol 455:125-145.
149
Pian P, Bucchi A, Robinson RB, Siegelbaum SA (2006) Regulation of getting and rundown of HCN hyperpolarization-activated channels by exogenous and endogenous PIP2. J Gen Physiol 128:593-604.
Picciotto MR, Higley MJ, Mineur YS (2012) Acetylcholine as a neuromodulator: Cholinergic signaling shapes nervous system function and behavior. Neuron 76:116-129.
Quilichini P, Sirota A, Buzsaki G (2010) Intrinsic circuit organization and theta-gamma oscillation dynamics in the entorhinal cortex of the rat. J Neurosci 30:11128-11142.
Raisman G, Cowan WM, Powell TP (1966) An experimental analysis of the efferent projection of the hippocampus. Brain 89:83-108.
Ray S, Naumann R, Burgalossi A, Tang Q, Schmidt H, Brecht M (2014) Grid-layout and thea- modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science 343:891- 896.
Rempel-Clower NL, Zola SM, Squire LR, Amaral DG (1996) Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci 16:5233-5255.
Richter M, Schilling T, Muller W (1999) Muscarinic control of intracortical connections to layer II in rat entorhinal cortex slice. Neurosci Lett 273:200-202.
Rolls ET (2013) The mechanisms for pattern completion and pattern separation in the hippocampus. Front Syst Neurosci 7:1-21.
Room P, Groenewegen HJ (1986) Connections of the parahippocampal cortex. I. Cortical afferents. J Comp Neurol 251:415-450.
Rosenkranz JA, Johnston D (2006) Dopaminergic regulation of neuronal excitability through modulation of Ih in layer V entorhinal cortex. J Neurosci 26:3229-3244.
Sanchez-Alonso JL, Halliwell JV, Colino A (2008) ZD 7288 inhibits T- type calcium current in rat hippocampal pyramidal cells. Neurosci Lett 439:275–280.
Santoro B, Chen S, Luthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA (2000). Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20:5264-5275.
Saudargiene A, Cobb S, Graham BP (2015) A computational study on plasticity during theta cycles at schaffer collateral synapses on CA1 pyramidal cells in the hippocampus. Hippocampus 25:208-218.
150
Scharfman HE, Goodman JH, Du F, Schwarcz R (1998) Chronic changes in synaptic responses of entorhinal and hippocampal neurons after amino-oxyacetic acid (AOAA) –induced entorhinal cortical neuron loss. J Neurophysiol 80:3031–3046.
Schenk F, Morris RGM (1985) Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions. Exp Brain Res 58:11-28.
Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21.
Shalinsky MH, Magistretti J, Ma L, Alonso AA (2002) Muscarinic activation of a cation current and associated current noise in entorhinal-cortex layer-II neurons. J Neurophysiol 88:1197–1211.
Shatz CJ (1992) The developing brain. Sci Am 267:60-67.
Shen W, Tian X, Day M, Ulrich S, Tkatch T, Nathanson NM, Surmeier, DJ (2007) Cholinergic
modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal
neurons. Nat Neurosci 11:1458-1466.
Shors TJ, Matzel LD (1997) Long-term potentiation: What’s learning got to do with it? Behav
Brain Sci 20:597-655.
Sjostrom PJ, Rancz EA, Roth A, Hausser M (2008) Dendritic excitability and synaptic plasticity.
Physiol Rev 88:769-840.
Solger J, Wozny C, Manahan-Vaughan D, Behr J (2004) Distinct mechanisms of bidirectional
activity-dependent synaptic plasticity in superficial and deep layers of rat entorhinal
cortex. Eur J Neurosci 19:2003-2007.
Sorensen KE, Shipley MT (1979) Projections from the subiculum to the deep layers of the
ipsilateral presubicular and entorhinal cortices in the guinea pig. J Comp Neurol 188:313-
333.
Sparks DW, Chapman CA (2013) Cholinergic receptor activation induces a relative facilitation
of synaptic responses in the entorhinal cortex during theta- and gamma-frequency
stimulation of parasubicular inputs. Neuroscience 230:72-85.
Sparks DW, Chapman CA (2014) Contribution of Ih to the relative facilitation of synaptic
responses induced by carbachol in the entorhinal cortex during repetitive stimulation of the parasubiculum. Neuroscience 278:81-92.
151
Spruston N (2008) Pyramidal neurons: Dendritic structure and synaptic integration. Nat Rev Neurosci 9:206-221.
Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu. Rev. Neurosci 27:279- 306.
Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380- 1386.
Staubli U, Otaky N (1994) Serotonin controls the magnitude of LTP induced by theta bursts via an action on NMDA-receptor- mediated responses. Brain Res 643:10–16.
Staubli U, Scafidi J, Chun D (1999) GABAB receptor antagonism: Facilitatory effects on memory parallels those on LTP induced by TBS but not HFS. J Neurosci 19:4609–4615.
Steffenach HA, Witter M, Moser MB, Moser EI (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301-313.
Sun C, Kitamura T, Yamamoto J, Martin J, Pignatelli M, Kitch LJ, Schnitzer MK, Tonegawa S (2015) Distinct speed dependence of entorhinal island and ocean cells, including respective grid cells. PNAS, 112:9466-9471.
Swanson LW, Cowan WM (1977) An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49084. Takehara-Nishiuchi K (2014) Entorhinal cortex and consolidated memory. Neurosci Res 84:27-
33.
Taube JS (1995) Place cells recorded in the parasubiculum of freely moving rats. Hippocampus
5:569–583.
Thompson RF (1976) The search for the engram. Am Psychol 31:209-227.
Thuault SJ, Malleret G, Constantinople CM, Nicholls R, Chen I, Zhu J, Panteleyev A, Vronskaya
S, Nolan MF, Bruno R, Siegelbaum SA, Kandel ER (2013) Prefrontal cortex HCN1 channels enable intrinsic persistent neural firing and executive memory function. J Neurosci 33:13583-13599.
Tamas G, Szabadics J, Lorincz A, Somogyi P (2004) Input and frequency-specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin. Eur J Neurosci 20:2681-2690.
Thiels E, Barrionuevo G, Berger T (1994) Excitatory stimulation during postsynaptic inhibition induces long-term depression in hippocampus in vivo. J Neurosci 15:3009-3116.
152
Tolner EA, Frahm C, Metzger R, Gorter JA, Witte OW, da Silva FHL, Heinemann U (2007) Synaptic responses in superficial layers of medial entorhinal cortex from rat with kainite- induced epilepsy. Neurobiol Dis 26:419–438.
Tsay D, Dudman JT, Siegelbaum SA (2007) HCN1 channels constrain synaptically evoked Ca2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 56:1076–1089.
Tsuno Y, Schultheiss NW, Hasselmo ME (2013) In vivo cholinergic modulation of the cellular properties of medial entorhinal cortex neurons. J Physiol 591:2611-2627.
van Groen T, Wyss JM (1990a) The connections of presubiculum and parasubiculum in the rat. Brain Res 518:227-243.
van Groen T, Wyss JM (1990b) Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 302:515-528.
van Hoesen GW (1995) Anatomy of the medial temporal lobe. Magn Reson Imaging 13:1047- 1055.
van Welie I, Remme MW, van Hooft JA, Wadman WJ (2006) Different levels of Ih determine distinct temporal integration in bursting and regular-spiking neurons in rat subiculum. J Physiol 576:203-214.
Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.
Witter MP (1993) Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 3:33-44.
Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33:161-253.
Witter MP, Moser EI (2006) Spatial representation and the architecture of the entorhinal cortex. Trends Neurosci 29:671-678.
Witter MP, Naber PA, van Haeften T, Machielsen WC, Rombouts SA, Barkhof F, Scheltens P, Lopes da Silva FH (2000b) Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10:398-410.
Witter MP, Wouterlood FG, Naber PA, van Haeften T (2000a) Anatomical organization of the parahippocampal-hippocampal network. Ann NY Acad Soci 911:1-24.
153
Woodhall G, Evans DI, Cunningham MO, Jones RS (2001) NR2B- containing NMDA autoreceptors at synapses on entorhinal cortical neurons. J Neurophysiol 86:1644–1651. Yamada WM, Zucker RS (1992) Time course of transmitter release calculated from simulations
of a calcium diffusion model. Biophys J 61:671-682.
Yamamoto J, Suh J, Takeuchi D, Tonegawa S (2014) Successful execution of working memory
linked to synchronized high- frequency gamma oscillations. Cell 157:845-857.
Yang CR, Seamans JK, Gorelova N (1996) Electrophysiolgical and morphological properties of
layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro. J Neurosci 16:1904-
1921.
Yejun H, Zorumski CF, Mennerick S (2002) Contribution of presynaptic Na+ channel
inactivation to paired-pulse synaptic depression in cultured hippocampal neurons. J
Neurophys 87:925-936.
Yi E, Roux I, Glowatzki E (2010) Dendritic HCN channels shape excitatory postsynaptic
potentials in the inner hair cell afferent synapse in the mammalian cochlea. J
Neurophysiol 103:2532-2543.
Ying SW, Jia F, Abbas SY, Hofmann F, Ludwig A, Goldstein PA (2007) Dendrtiic HCN2
channels constrain glutamate-driven excitability in reticular thalamic neurons. J Neurosci
27:7819-8732.
Yoshida M, Alonso A (2007) Cell-type-specific modulation of intrinsic firing properties and
subthreshold membrane oscillations by the M(Kv7)-current in neurons of the entorhinal
cortex. J Neurophysiol 98:2779–2794.
Yun SH, Cheong MY, Mook-Jung I, Huh K, Lee CJ, Jung MW (2000) Cholinergic modulation
of synaptic transmission and plasticity in entorhinal cortex and hippocampus of the rat.
Neuroscience 97:671-676.
Yun SH, Mook-Jung I, Jung MW (2002) Variation in effective stimulus patterns for induction of
long-term potentiation across different layers of rat entorhinal cortex. J Neurosci
22:RC214.
Zhu Y, Wang R (2016) A comparative study of the impact of theta-burst and high-frequency
stimulation on memory performance. Front Hum Neurosci 10:19.
154
Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950-2967.
Zola-Morgan S, Squire LR (1990) The neuropsychology of memory: Parallel findings in humans and nonhuman primates. Ann NY Acad Sci 608:434-450.
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