Axonal Activity in vivo: Technical considerations and implications for the exploration of neural circuits in freely moving animals

Frontiers in Neuroscience

Volumn 9, Issue APR, 2015, Pages

  Barry, Jeremy M ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ATTENTION; BRAIN REGION; CLASSIFICATION; CONNECTOME; EPILEPSY; IN VIVO STUDY; INFORMATION PROCESSING; INTERNEURON; LEARNING; MEDIAL ENTORHINAL CORTEX; MEMORY; MENTAL DISEASE; NERVE CONDUCTION; NERVE ENDING; NERVE FIBER; NERVE FIBER MEMBRANE; NONHUMAN; NONMYELINATED NERVE; REVIEW; SHORT DURATION WAVEFORM; SPIKE WAVE; THALAMUS RETICULAR NUCLEUS; WAVEFORM;

EID: 84928685960     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00153     Document Type: Review

References (76)

1. Amassian VE, Macy J, Jr., Waller HJ (1961) Patterns of activity of simultaneously recorded neurons in midbrain reticular formation. Ann N Y Acad Sci 89:883-895.
2. Bakkum DJ, Frey U, Radivojevic M, Russell TL, Muller J, Fiscella M, Takahashi H, Hierlemann A (2013) Tracking axonal action potential propagation on a highdensity microelectrode array across hundreds of sites. Nat Commun 4:2181.
3. Ballo AW, Bucher D (2009) Complex intrinsic membrane properties and dopamine shape spiking activity in a motor axon. J Neurosci 29:5062-5074.
4. Ballo AW, Nadim F, Bucher D (2012) Dopamine modulation of Ih improves temporal fidelity of spike propagation in an unmyelinated axon. J Neurosci 32:5106-5119.
5. Ballo AW, Keene JC, Troy PJ, Goeritz ML, Nadim F, Bucher D (2010) Dopamine modulates Ih in a motor axon. J Neurosci 30:8425-8434.
6. Bartho P, Slezia A, Matyas F, Faradzs-Zade L, Ulbert I, Harris KD, Acsady L (2014) Ongoing network state controls the length of sleep spindles via inhibitory activity. Neuron 82:1367-1379.
7. Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209-219.
8. 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.
9. Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB (2008) Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57:290-302.
10. Bucher D, Goaillard JM (2011) Beyond faithful conduction: short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon. Prog Neurobiol 94:307-346.
11. Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.
12. Carandini M, Shimaoka D, Rossi LF, Sato TK, Benucci A, Knopfel T (2015) Imaging the awake visual cortex with a genetically encoded voltage indicator. J Neurosci 35:53-63.
13. Chang EH, Frattini SA, Robbiati S, Huerta PT (2013) Construction of microdrive arrays for chronic neural recordings in awake behaving mice. Journal of visualized experiments: JoVE:e50470.
14. Cho J, Sharp PE (2001) Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 115:3-25.
15. Chung K, Wallace J, Kim SY, Kalyanasundaram S, Andalman AS, Davidson TJ, Mirzabekov JJ, Zalocusky KA, Mattis J, Denisin AK, Pak S, Bernstein H, Ramakrishnan C, Grosenick L, Gradinaru V, Deisseroth K (2013) Structural and molecular interrogation of intact biological systems. Nature 497:332-337.
16. Colgin LL, Moser EI (2010) Gamma oscillations in the hippocampus. Physiology (Bethesda) 25:319-329.
17. Cooper GF, Robson JG, Waldron I (1969) The action potentials recorded from undamaged nerve fibres with micro-electrodes. J Physiol 200:9P-11P.
18. Debanne D (2004) Information processing in the axon. Nat Rev Neurosci 5:304-316
19. Deller T, Adelmann G, Nitsch R, Frotscher M (1996) The alvear pathway of the rat hippocampus. Cell Tissue Res 286:293-303.
20. Dugladze T, Schmitz D, Whittington MA, Vida I, Gloveli T (2012) Segregation of axonal and somatic activity during fast network oscillations. Science 336:1458-1461.
21. Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476-2489.
22. Fenton AA, Lytton WW, Barry JM, Lenck-Santini PP, Zinyuk LE, Kubik S, Bures J, Poucet B, Muller RU, Olypher AV (2010) Attention-like modulation of hippocampus place cell discharge. J Neurosci 30:4613-4625.
23. Fox SE, Ranck JB, Jr. (1975) Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats. Exp Neurol 49:299-313.
24. Fox SE, Ranck JB, Jr. (1981) Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res 41:399-410.
25. Gloveli T, Dugladze T, Rotstein HG, Traub RD, Monyer H, Heinemann U, Whittington MA, Kopell NJ (2005) Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus. Proc Natl Acad Sci U S A 102:13295-13300.
26. Graham B (2014) Modeling the Axon. In: Encyclopedia of Computational Neuroscience (Jaeger D, Jung R, eds), pp 1-9: Springer New York.
27. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801-806.
28. Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI (2008) Hippocampus-independent phase precession in entorhinal grid cells. Nature 453:1248-1252.
29. Henze DA, Borhegyi Z, Csicsvari J, Mamiya A, Harris KD, Buzsaki G (2000) Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J Neurophysiol 84:390-400.
30. Hu W, Shu Y (2012) Axonal bleb recording. Neurosci Bull 28:342-350.
31. Huxter J, Burgess N, O'Keefe J (2003) Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425:828-832.
32. Insel N, Barnes CA (2014) Differential Activation of Fast-Spiking and Regular-Firing Neuron Populations During Movement and Reward in the Dorsal Medial Frontal Cortex. Cereb Cortex.
33. Johnston D, Wu SM-s (1995) Foundations of cellular neurophysiology. Cambridge, Mass.: MIT Press.
34. Kamondi A, Acsady L, Wang XJ, Buzsaki G (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phaseprecession of action potentials. Hippocampus 8:244-261.
35. Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER (2004) Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42:283-295.
36. Kleen JK, Scott RC, Holmes GL, Lenck-Santini PP (2010) Hippocampal interictal spikes disrupt cognition in rats. Ann Neurol 67:250-257.
37. Kole MH, Letzkus JJ, Stuart GJ (2007) Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55:633-647.
38. Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7:548-562.
39. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966.
40. Leutgeb S, Ragozzino KE, Mizumori SJ (2000) Convergence of head direction and place information in the CA1 region of hippocampus. Neuroscience 100:11-19.
41. Meeks JP, Jiang X, Mennerick S (2005) Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus. J Physiol 566:425-441.
42. Mizumori SJ, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015-4028.
43. Monsivais P, Clark BA, Roth A, Hausser M (2005) Determinants of action potential propagation in cerebellar Purkinje cell axons. J Neurosci 25:464-472.
44. Mountcastle VB, Talbot WH, Sakata H, Hyvarinen J (1969) Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol 32:452-484.
45. Muzzio IA, Kentros C, Kandel E (2009) What is remembered? Role of attention on the encoding and retrieval of hippocampal representations. J Physiol 587:2837-2854.
46. Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53-83.
47. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford New York: Clarendon Press; Oxford University Press.
48. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
49. Penttonen M, Kamondi A, Acsady L, Buzsaki G (1998) Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci 10:718-728.
50. Popovic M, Gao X, Zecevic D (2012) Voltage-sensitive dye recording from axons, dendrites and dendritic spines of individual neurons in brain slices. Journal of visualized experiments: JoVE:e4261.
51. Preston RJ, Waxman SG, Kocsis JD (1983) Effects of 4-aminopyridine on rapidly and slowly conducting axons of rat corpus callosum. Exp Neurol 79:808-820.
52. Raastad M, Shepherd GM (2003) Single-axon action potentials in the rat hippocampal cortex. J Physiol 548:745-752.
53. Ramón y Cajal S (1953) Histologie du système nerveux de l'homme & des vertébrés, éd. française rev. & mise à jour Edition. Madrid,: Consejo Superior de Investigaciones Científicas, Instituto Ramón y Cajal.
54. Ranck JB, Jr. (1973) Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41:461-531.
55. Robbins AA, Fox SE, Holmes GL, Scott RC, Barry JM (2013) Short duration waveforms recorded extracellularly from freely moving rats are representative of axonal activity. Front Neural Circuits 7:181.
56. Segev I, Schneidman E (1999) Axons as computing devices: basic insights gained from models. J Physiol Paris 93:263-270.
57. Shu Y, Duque A, Yu Y, Haider B, McCormick DA (2007) Properties of action-potential initiation in neocortical pyramidal cells: evidence from whole cell axon recordings. J Neurophysiol 97:746-760.
58. Singer W (2011) Dynamic formation of functional networks by synchronization. Neuron 69:191-193.
59. Sturrock RR (1980) Myelination of the mouse corpus callosum. Neuropathology and applied neurobiology 6:415-420.
60. Swadlow HA, Waxman SG, Geschwind N (1980a) Small-diameter nonmyelinated axons in the primate corpus callosum. Archives of neurology 37:114-115.
61. Swadlow HA, Kocsis JD, Waxman SG (1980b) Modulation of impulse conduction along the axonal tree. Annu Rev Biophys Bioeng 9:143-179.
62. Swanson TH, Krahl SE, Liu YZ, Drazba JA, Rivkees SA (1998) Evidence for physiologically active axonal adenosine receptors in the rat corpus callosum. Brain Res 784:188-198.
63. Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70-86.
64. Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181-207.
65. Tomassy GS, Berger DR, Chen HH, Kasthuri N, Hayworth KJ, Vercelli A, Seung HS, Lichtman JW, Arlotta P (2014) Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344:319-324.
66. Traub RD, Cunningham MO, Gloveli T, LeBeau FE, Bibbig A, Buhl EH, Whittington MA (2003a) GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations. Proc Natl Acad Sci U S A 100:11047-11052.
67. Traub RD, Pais I, Bibbig A, LeBeau FE, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA (2003b) Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc Natl Acad Sci U S A 100:1370-1374.
68. Vigneswaran G, Kraskov A, Lemon RN (2011) Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification. J Neurosci 31:14235-14242.
69. Waxman SG, Swadlow HA (1976) Ultrastructure of visual callosal axons in the rabbit. Exp Neurol 53:115-127.
70. Wiener SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13:3802-3817.
71. Witter MP, Moser EI (2006) Spatial representation and the architecture of the entorhinal cortex. Trends Neurosci 29:671-678.
72. Womelsdorf T, Fries P (2007) The role of neuronal synchronization in selective attention. Curr Opin Neurobiol 17:154-160.
73. Xia Y, Zhao Y, Yang M, Zeng S, Shu Y (2014) Regulation of action potential waveforms by axonal GABAA receptors in cortical pyramidal neurons. PLoS One 9:e100968.
74. Yang J, Ye M, Tian C, Yang M, Wang Y, Shu Y (2013) Dopaminergic modulation of axonal potassium channels and action potential waveform in pyramidal neurons of prefrontal cortex. J Physiol 591:3233-3251.
75. Zalesky A, Fornito A, Seal ML, Cocchi L, Westin CF, Bullmore ET, Egan GF, Pantelis C (2011) Disrupted axonal fiber connectivity in schizophrenia. Biol Psychiatry 69:80-89.
76. Zhang SJ, Ye J, Couey JJ, Witter M, Moser EI, Moser MB (2014) Functional connectivity of the entorhinal-hippocampal space circuit. Philos Trans R Soc Lond B Biol Sci 369:20120516.