Distinct Functional Groups Emerge from the Intrinsic Properties of Molecularly Identified Entorhinal Interneurons and Principal Cells

Cerebral Cortex

Volumn 27, Issue 6, 2017, Pages 3186-3207

  Ferrante, Michele ^a   Tahvildari, Babak ^b,c   Duque, Alvaro ^b,c   Hadzipasic, Muhamed ^c   Salkoff, David ^b,c   Zagha, Edward William ^b,c   Hasselmo, Michael E ^a   McCormick, David A ^b,c  

^a BOSTON UNIVERSITY   (United States)

^b Boston University ^*  (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cell functional classification; entorhinal cortex; grid cells; interneurons; intrinsic properties

Indexed keywords

CALRETININ; PARVALBUMIN; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE; DNA BINDING PROTEIN; DSCR1L1 PROTEIN, MOUSE; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; GRHL3 PROTEIN, MOUSE; NEUROPEPTIDE Y; PROTEIN; SEROTONIN 3 RECEPTOR; TRANSCRIPTION FACTOR;

ACCURACY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL COUNT; CELL LEVEL; CELL STRUCTURE; COMPARATIVE STUDY; CONDUCTANCE; CONTROLLED STUDY; DECISION TREE; ELECTRIC POTENTIAL; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MEMBRANE STEADY POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; STEADY STATE; STELLATE CELL; WHOLE CELL PATCH CLAMP; ANIMAL; BIOPHYSICS; CLASSIFICATION; CLUSTER ANALYSIS; CYTOLOGY; ELECTROSTIMULATION; GENETICS; IN VITRO STUDY; MEMBRANE POTENTIAL; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BIOPHYSICS; CELL COUNT; CLUSTER ANALYSIS; DNA-BINDING PROTEINS; ELECTRIC STIMULATION; ENTORHINAL CORTEX; GREEN FLUORESCENT PROTEINS; IN VITRO TECHNIQUES; INTERNEURONS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; NEUROPEPTIDE Y; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; PROTEINS; RECEPTORS, SEROTONIN, 5-HT3; TRANSCRIPTION FACTORS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 85026885435     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhw143     Document Type: Article

References (135)

1. Alitto HJ, Dan Y. 2013. Cell-type-specific modulation of neocortical activity by basal forebrain input. Front Syst Neurosci. 6:79.
2. Alonso A, Klink R. 1993. Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol. 70(1):128-143.
3. Alonso A, Llinás RR. 1989. Subthreshold Na+-dependent thetalike rhythmicity in stellate cells of entorhinal cortex layer II. Nature. 342(6246):175-177.
4. Armañanzas R, Ascoli GA. 2015. Towards the automatic classification of neurons. Trends Neurosci. 38(5):307-318.
5. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairén A, et al. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci. 9:557-568.
6. Ascoli GA, Donohue DE, Halavi M. 2007. NeuroMorpho. Org: A central resource for neuronal morphologies. J Neurosci. 27 (35):9247-9251.
7. Beed P, Gundlfinger A, Schneiderbauer S, Song J, Böhm C, Burgalossi A, Brecht M, Vida I, Schmitz D. 2013. Inhibitory gradient along the dorsoventral axis in the medial entorhinal cortex. Neuron. 79(6):1197-1207.
8. Bezaire MJ, Soltesz I. 2013. Quantitative assessment of CA1 local circuits: knowledge base for interneuron-pyramidal cell connectivity. Hippocampus. 23(9):751-785.
9. Boehlen A, Heinemann U, Erchova I. 2010. The range of intrinsic frequencies represented by medial entorhinal cortex stellate cells extends with age. J Neurosci. 30:4585-4589.
10. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME. 2011. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science. 332(6029):595-599.
11. Brandon MP, Bogaard AR, Schultheiss NW, Hasselmo ME. 2013. Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat Neurosci. 16(6):739-748.
12. Breiman L, Friedman JH, Olshen RA, Stone CJ. 1984. Classification and Regression Trees. Belmont, CA: Wadsworth.
13. Brock G, Pihur V, Datta S, Datta S. 2008. clValid: An R Package for Cluster Validation. J Stat Softw. 25(4). Available from: URL http://www. jstatsoft. org/v25/i04 (24May 2016, date last accessed).
14. Buckmaster PS, Alonso A, Canfield DR, Amaral DG. 2004. Dendritic morphology, local circuitry, and intrinsic electrophysiology of principal neurons in the entorhinal cortex of macaque monkeys. J Comp Neurol. 470(3):317-329.
15. Buetfering C, Allen K, Monyer H. 2014. Parvalbumin interneurons provide grid cell-driven recurrent inhibition in the medial entorhinal cortex. Nat Neurosci. 17(5):710-718.
16. Burak Y, Fiete IR. 2009. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol. 5: e1000291.
17. Burgess N, Barry C, O'Keefe J. 2007. An oscillatory interference model of grid cell firing. Hippocampus. 17:801-812.
18. Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G. 2005. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron. 48 (4):591-604.
19. Buzsaki G, Moser EI. 2013. Memory, navigation and theta rhythmin the hippocampal-entorhinal system. Nat Neurosci. 16:130-138.
20. Cannon RC, Turner DA, Pyapali GK, Wheal HV. 1998. An on-line archive of reconstructed hippocampal neurons. J Neurosci Methods. 84(1-2):49-54.
21. Canto CB, Witter MP. 2012a. Cellular properties of principal neurons in the rat entorhinal cortex. II. The medial entorhinal cortex. Hippocampus. 22(6):1277-1299.
22. Canto CB, Witter MP. 2012b. Cellular properties of principal neurons in the rat entorhinal cortex. I. The lateral entorhinal cortex. Hippocampus. 22(6):1256-1276.
23. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 459 (7247):663-667.
24. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. 1997. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature. 389(6653):816-824.
25. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J. 1997. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci. 17(10):3894-3906.
26. Chen J, Sroubek J, Krishnan Y, Li Y, Bian J, McDonald TV. 2009. PKA phosphorylation of HERG protein regulates the rate of channel synthesis. Am J Physiol Heart Circ Physiol. 296: H1244-H1254.
27. Chittajallu R, Craig MT, McFarland A, Yuan X, Gerfen S, Tricoire L, Erkkila B, Barron SC, Lopez CM, Liang BJ, et al. 2013. Dual origins of functionally distinct O-LM interneurons revealed by differential 5-HT(3A)R expression. Nat Neurosci. 16(11):1598-1607.
28. Cho H, Yang YD, Lee J, Lee B, Kim T, Jang Y, Back SK, Na HS, Harfe BD, Wang F, et al. 2012. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat Neurosci. 15(7):1015-1021.
29. Chowdhury S, Jarecki BW, Chanda B. 2014. A molecular framework for temperature-dependent gating of ion channels. Cell. 158(5):1148-1158.
30. Clapham DE. 2003. TRP channels as cellular sensors. Nature. 426 (6966):517-524.
31. Climer JR, Newman EL, Hasselmo ME. 2013. Phase coding by grid cells in unconstrained environments: Two-dimensional phase precession. Eur J Neurosci. 38:2526-2541.
32. Cobos I, Long JE, Thwin MT, Rubenstein JL. 2006. Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb Cortex. 16(Suppl 1):i82-i88.
33. Connor JR, Peters A. 1984. Vasoactive intestinal polypeptideimmunoreactive neurons in rat visual cortex. Neuroscience. 12(4):1027-1044.
34. Couey JJ, Witoelar A, Zhang SJ, Zheng K, Ye J, Dunn B, Czajkowski R, Moser MB, Moser EI, Roudi Y, et al. 2013. Recurrent inhibitory circuitry as a mechanism for grid formation. Nat Neurosci. 16(3):318-324.
35. Craig MT, McBain CJ. 2015. Navigating the circuitry of the brain's GPS system: future challenges for neurophysiologists. Hippocampus. 25(6):736-743.
36. DeCoursey TE, Cherny VV. 1998. Temperature dependence of voltage-gated H+ currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J Gen Physiol. 112(4):503-522.
37. Destexhe A, Hughes SW, Rudolph M, Crunelli V. 2010. Are corticothalamic UP states fragments of wakefulness Trends Neurosci. 30(7):334-342.
38. Dib-Hajj SD, Yang Y, Waxman SG. 2008. Genetics and molecular pathophysiology of Na(v)1. 7-related pain syndromes. Adv Genet. 63:85-110.
39. Dickson CT, Magistretti J, Shalinsky MH, Fransén E, Hasselmo ME, Alonso A. 2000. Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J Neurophysiol. 83(5):2562-2579.
40. Dickson CT, Mena AR, Alonso A. 1997. Electroresponsiveness of medial entorhinal cortex layer III neurons in vitro. Neuroscience. 81(4):937-950.
41. Doischer D, Hosp JA, Yanagawa Y, Obata K, Jonas P, Vida I, Bartos M. 2008. Postnatal differentiation of basket cells from slow to fast signaling devices. J Neurosci. 28(48):12956-12968.
42. Domnisoru C, Kinkhabwala AA, Tank DW. 2013. Membrane potential dynamics of grid cells. Nature. 495(7440):199-204.
43. Dunstan RW, Wharton KA Jr, Quigley C, Lowe A. 2011. The use of immunohistochemistry for biomarker assessment-can it compete with other technologies Toxicol Pathol. 39 (6):988-1002.
44. Duque A, Gazula V, Kaczmarek LK. 2013. Expression of Kv1. 3 potassium channels regulates density of cortical interneurons. Dev Neurobiol. 73(11):10. 1002.
45. Eggink H, Mertens P, Storm E, Giocomo LM. 2013. Hyperpolarization-activated cyclic nucleotide-gated 1 independent grid cell-phase precession in mice. Hippocampus. 24:249-256.
46. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA. 2002. Graded persistent activity in entorhinal cortex neurons. Nature. 420:173-178.
47. Erchova I, Kreck G, Heinemann U, Herz AV. 2004. Dynamics of rat entorhinal cortex layer II and III cells: characteristics of membrane potential resonance at rest predict oscillation properties near threshold. J Physiol. 560(Pt 1):89-110.
48. Ferrante M. 2012. Dynamical Multiscale Models to Formulate Testable Predictions of Neuronal Computational Properties. Ph. D. Dissertation. George Mason Univ., Fairfax, VA, USA. Advisor Giorgio A. Ascoli. AAI3503977, ISBN: 978-1-267-27837-1.
49. Ferrante M, Ascoli GA. 2015. Distinct and synergistic feedforward inhibition of pyramidal cells by basket and bistratified interneurons. Front Cell Neurosci. 9:439.
50. Ferrante M, Blackwell KT, Migliore M, Ascoli GA. 2008. Computational models of neuronal biophysics and the characterization of potential neuropharmacological targets. Curr Med Chem. 15(24):2456-2471.
51. Ferrante M, Migliore M, Ascoli GA. 2009. Feed-forward inhibition as a buffer of the neuronal input-output relation. Proc Natl Acad Sci USA. 106(42):18004-9.
52. Ferrante M, Migliore M, Ascoli GA. 2013. Functional impact of dendritic branch-point morphology. J Neurosci. 33(5): 2156-2165.
53. Ferrante M, Shay CF, Tsuno Y, William Chapman G, Hasselmo ME. 2016. Post-inhibitory rebound spikes in rat medial entorhinal layer II/III principal cells: in vivo, in vitro, and computational modeling characterization. Cereb Cortex. 129:83-98.
54. Fishell G, Rudy B. 2011. Mechanisms of inhibition within the telencephalon: "where the wild things are". Annu Rev Neurosci. 34:535-567.
55. Fransén E, Tahvildari B, Egorov AV, Hasselmo ME, Alonso AA. 2006. Mechanism of graded persistent cellular activity of entorhinal cortex layer v neurons. Neuron. 49(5):735-746.
56. Fu Y, Tucciarone JM, Espinosa JS, Sheng N, Darcy DP, Nicoll RA, Huang ZJ, Stryker MP. 2014. A cortical circuit for gain control by behavioral state. Cell. 156:1139-1152.
57. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. 2004. Spatial representation in the entorhinal cortex. Science. 305 (5688):1258-1264.
58. Garden DL, Dodson PD, O'Donnell 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 (5):875-889.
59. Giocomo LM, Hasselmo ME. 2009. Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adult mice. J Neurosci. 29(23):7625-7630.
60. Giocomo LM, Hussaini SA, Zheng F, Kandel ER, Moser MB, Moser EI. 2011a. Grid cells use hcn1 channels for spatial scaling. Cell. 147:1159-1170.
61. Giocomo LM, Moser M-B, Moser EI. 2011b. Computational models of grid cells. Neuron. 71:589-603.
62. 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.
63. Goldberg EM, Clark BD, Zagha E, Nahmani M, Erisir A, Rudy B. 2008. K+ channels at the axon initial segment Dampen nearthreshold excitability of neocortical fast-spiking GABAergic interneurons neuron. Neuron. 58(3):387-400.
64. Gonchar Y, Wang Q, Burkhalter A. 2008. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat. 1:3.
65. Gonzalez-Sulser A, Parthier D, Candela A, McClure C, Pastoll H, Garden D, Sürmeli G, Nolan MF. 2014. GABAergic projections from the medial septum selectively inhibit interneurons in the medial entorhinal cortex. J Neurosci. 34(50):16739-16743.
66. Guerra L, McGarry LM, Robles V, Bielza C, Larrañaga P, Yuste R. 2011. Comparison between supervised and unsupervised classifications of neuronal cell types: A case study. Dev Neurobiol. 71(1):71-82.
67. Haas JS, White JA. 2002. Frequency selectivity of layer II stellate cells in the medial entorhinal cortex. J Neurophysiol. 88:2422-2429.
68. Hadzipasic M, Tahvildari B, Nagy M, Bian M, Horwich AL, McCormick DA. 2014. Selective degeneration of a physiological subtype of spinal motor neuron in mice with SOD1-linked ALS. Proc Natl Acad Sci USA. 111(47):16883-8.
69. Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI. 2008. Hippocampus-independent phase precession in entorhinal grid cells. Nature. 453(7199):1248-1252.
70. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature. 436(7052):801-806.
71. Hajós F, Zilles K, Schleicher A, Kálmán M. 1988. Types and spatial distribution of vasoactive intestinal polypeptide (VIP)-containing synapses in the rat visual cortex. Anat Embryol (Berl). 178(3):207-217.
72. Hájos N, Mody I. 2009. Establishing a physiological environment for visualized in vitro brain slice recordings by increasing oxygen supply and modifying aCSF content. J Neurosci Methods. 183(2):107-113.
73. Hasselmo ME. 2013. Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex. Philos Trans R Soc Lond B Biol Sci. 369(1635):20120523.
74. Hasselmo ME, Shay CF. 2014. Grid cell firing patterns may arise from feedback interaction between intrinsic rebound spiking and transverse traveling waves with multiple heading angles. Front Syst Neurosci. 8:201.
75. Hasselmo ME, Stern CE. 2015. Current questions on space and time encoding. Hippocampus. 25(6):744-752.
76. Hochbaum DR, Zhao Y, Farhi SL, Klapoetke N, Werley CA, Kapoor V, Zou P, Kralj JM, Maclaurin D, Smedemark-Margulies N, et al. 2014. All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat Methods. 11(8):825-833.
77. Hu H, Gan J, Jonas P. 2014. Interneurons. Fast-spiking, parvalbumin+ GABAergic interneurons: from cellular design to microcircuit function. Science. 345(6196):1255263.
78. Hutcheon B, Yarom Y. 2000. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23(5):216-222.
79. Ibáñez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koós T, Tepper JM. 2011. A novel functionally distinct subtype of striatal neuropeptide Y interneuron. J Neurosci. 31 (46):16757-16769.
80. Johnson SM, Felder RB. 1993. Effects of aging on the intrinsic membrane properties of medial NTS neurons of Fischer-344 rats. J Neurophysiol. 70(5):1975-1987.
81. Karagiannis A, Gallopin T, Dávid C, Battaglia D, Geoffroy H, Rossier J, Hillman EM, Staiger JF, Cauli B. 2009. Classification of NPY-expressing neocortical interneurons. J Neurosci. 29 (11):3642-3659.
82. Karnani MM, Agetsuma M, Yuste R. 2014. A blanket of inhibition: functional inferences from dense inhibitory connectivity. Curr Opin Neurobiol. 26:96-102.
83. Kawaguchi Y, Katsumaru H, Kosaka T, Heizmann CW, Hama K. 1987. Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416(2):369-374.
84. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex. 7 (6):476-486.
85. Kawaguchi Y, Kubota Y. 1996. Physiological and morphological identification of somatostatin-or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci. 16(8):2701-2715.
86. Keshavarzi S, Sullivan RK, Ianno DJ, Sah P. 2014. Functional properties and projections of neurons in the medial amygdala. J Neurosci. 34(26):8699-8715.
87. Klausberger T, Marton LF, O'Neill J, Huck JH, Dalezios Y, Fuentealba P, Suen WY, Papp E, Kaneko T, Watanabe M, et al. 2005. Complementary roles of cholecystokinin-and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J Neurosci. 25(42):9782-9793.
88. Klink R, Alonso A. 1997. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol. 77(4):1829-1843.
89. Krimer LS, Zaitsev AV, Czanner G, Kröner S, González-Burgos G, Povysheva NV, Iyengar S, Barrionuevo G, Lewis DA. 2005. Cluster analysis-based physiological classification andmorphological properties of inhibitory neurons in layers 2-3 of monkey dorsolateral prefrontal cortex. J Neurophysiol. 94(5):3009-3022.
90. Kubota Y, Hattori R, Yui Y. 1994. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res. 649:159-173.
91. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. 2010. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci. 30 (50):16796-16808.
92. Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B. 2013. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neurosci. 16:1662-1670.
93. Magistretti PJ, Morrison JH. 1998. Noradrenaline-and vasoactive intestinal peptide-containing neuronal systems in neocortex: functional convergence with contrasting morphology. Neuroscience. 24:367-378.
94. Maingret F, Lauritzen I, Patel AJ, Heurteaux C, Reyes R, Lesage F, Lazdunski M, Honoré E. 2000. TREK-1 is a heat-activated background K(+) channel. EMBO J. 19(11):2483-2491.
95. McCormick DA, Connors BW, Lighthall JW, Prince DA. 1985. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 54 (4):782-806.
96. McKemy DD, Neuhausser WM, Julius D. 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature. 416(6876):52-58.
97. Migliore M, Ferrante M, Ascoli GA. 2005. Signal propagation in oblique dendrites of CA1 pyramidal cells. J Neurophysiol. 94 (6):4145-4155.
98. Migliore M, Messineo L, Ferrante M. 2004. Dendritic Ih selectively blocks temporal summation of unsynchronized distal inputs in CA1 pyramidal neurons. J Comput Neurosci. 16(1):5-13.
99. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G. 2010. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci. 30(5):1582-1594.
100. Mizuseki K, Sirota A, Pastalkova E, Buzsaki G. 2009. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron. 64 (2):267-280.
101. Moran MM, Xu H, Clapham DE. 2004. TRP ion channels in the nervous system. Curr Opin Neurobiol. 14(3):362-369.
102. Nery S, Fishell G, Corbin JG. 2002. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci. 5(12):1279-1287.
103. Newman EL, Climer JR, Hasselmo ME. 2014. Grid cell spatial tuning reduced following systemic muscarinic receptor blockade. Hippocampus. 24:643-655.
104. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW. 2000. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci. 20(9):3354-3368.
105. Patapoutian A, Peier AM, Story GM, Viswanath V. 2003. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci. 4(7):529-539.
106. Perez-Rosello T, Baker JL, Ferrante M, Iyengar S, Ascoli GA, Barrionuevo G. 2011. Passive and active shaping of unitary responses from associational/commissural and perforant path synapses in hippocampal CA3 pyramidal cells. J Comput Neurosci. 31(2):159-182.
107. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B. 2003. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA. 100 (23):13638-13643.
108. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M. 2013. Inhibition of inhibition in visual cortex: The logic of connections between molecularly distinct interneurons. Nat Neurosci. 16 (8):1068-1076.
109. Pi HJ, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A. 2013. Cortical interneurons that specialize in disinhibitory control. Nature. 503:521-524.
110. Pike FG, Goddard RS, Suckling JM, Ganter P, Kasthuri N, Paulsen O. 2000. Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents. J Physiol. 529(Pt 1):205-213.
111. Porter JT, Cauli B, Staiger JF, Lambolez B, Rossier J, Audinat E. 1998. Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex. Eur J Neurosci. 10:3617-3628.
112. Pouille F, Marin-Burgin A, Adesnik H, Atallah BV, Scanziani M. 2009. Input normalization by global feedforward inhibition expands cortical dynamic range. Nat Neurosci. 12(12): 1577-1585.
113. Pusch M, Ludewig U, Jentsch TJ. 1997. Temperature dependence of fast and slow gating relaxations of ClC-0 chloride channels. J Gen Physiol. 109(1):105-116.
114. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. 2011. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol. 71(1):45-61.
115. Salkoff DB, Zagha E, Yüzgeç Ö, McCormick DA. 2015. Synaptic mechanisms of tight spike synchrony at gamma frequency in cerebral cortex. J Neurosci. 35(28):10236-10251.
116. Sanchez-Vives MV, McCormick DA. 2000. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 3(10):1027-1034.
117. Santi CM, Ferreira G, Yang B, Gazula VR, Butler A, Wei A, Kaczmarek LK, Salkoff L. 2006. Opposite regulation of Slick and Slack K+ channels by neuromodulators. J Neurosci. 26:5059-5068.
118. Shay CF, Ferrante M, Chapman GW, Hasselmo ME. 2015. Rebound Spiking in Layer II Medial Entorhinal Cortex Stellate Cells: Possible Mechanism of Grid Cell Function. Neurobiol Learn Mem. doi:10. 1016/j. nlm. 2015. 09. 004.
119. Siddiq A, Miyazaki T, Takagishi Y, Kanou Y, Hayasaka S, Inouye M, Seo H, Murata Y. 2001. Expression of ZAKI-4 messenger ribonucleic acid in the brain during rat development and the effect of hypothyroidism. Endocrinology. 142(5):1752-1759.
120. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science. 322(5909):1865-1868.
121. Sosulina L, Meis S, Seifert G, Steinhäuser C, Pape HC. 2006. Classification of projection neurons and interneurons in the rat lateral amygdala based upon cluster analysis. Mol Cell Neurosci. 33(1):57-67.
122. Steriade M, Nuñez A, Amzica F. 1993. A novel slow (>1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci. 13(8):3252-3265.
123. Steriade M, Timofeev I, Grenier F. 2001. Natural waking and sleep states: A viewfrominside neocortical neurons. J Neurophysiol. 85(5):1969-1985.
124. Suzuki WA. 2010. Untangling memory from perception in the medial temporal lobe. Trends Cogn Sci. 14(5):195-200.
125. Tahvildari B, Alonso A. 2005. Morphological and electrophysiological properties of lateral entorhinal cortex layers II and III principal neurons. J Comp Neurol. 491(2):123-140.
126. Tahvildari B, Alonso AA, BourqueCW. 2008. Ionic basis of ON and OFF persistent activity in layer III lateral entorhinal cortical principal neurons. J Neurophysiol. 99(4):2006-2011.
127. Tahvildari B, Fransén E, Alonso AA, Hasselmo ME. 2007. Switching between "On" and "Off" states of persistent activity in lateral entorhinal layer III neurons. Hippocampus. 17(4):257-263.
128. Tahvildari B, Wölfel M, Duque A, McCormick DA. 2012. Selective functional interactions between excitatory and inhibitory cortical neurons and differential contribution to persistent activity of the slow oscillation. J Neurosci. 32(35):12165-12179.
129. Tang Q, Burgalossi A, Ebbesen CL, Ray S, Naumann R, Schmidt H, Spicher D, Brecht M. 2014. Pyramidal and stellate cell specificity of grid and border representations in layer 2 of medial entorhinal cortex. Neuron. 84(6):1191-1197.
130. Tsuno Y, Chapman GW, Hasselmo ME. 2015. Rebound spike properties of medial entorhinal cortex neurons in vivo. Eur J Neurosci. 42(11):2974-2984.
131. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, et al. 2008. Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex. 18(2):315-330.
132. Vandenberg JI, Varghese A, Lu Y, Bursill JA, Mahaut-Smith MP, Huang CL. 2006. Temperature dependence of human ethera-go-go-related gene K+ currents. Am J Physiol Cell Physiol. 291(1):C165-C175.
133. Ward JH Jr. 1963. Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 58(301):236-244.
134. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA. 2004. Origins of cortical interneuron subtypes. J Neurosci. 24 (11):2612-2622.
135. Xu H, Jeong HY, Tremblay R, Rudy B. 2013. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron. 77(1):155-167.