Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility

Dunn, Soraya L. S.; Town, Stephen M.; Bizley, Jennifer K.; Bendor, Daniel

doi:10.1038/s41467-022-33507-2

Cited by 17Memory and Neural MechanismsNeural dynamics and brain functionNeuroscience and Neuropharmacology Research

Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility

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Dunn, Soraya L. S., Town, Stephen M., Bizley, Jennifer K., Bendor, Daniel·2022·Nature Communications

DOI 10.1038/s41467-022-33507-2PMC PMC9547075

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Abstract

Theta oscillations are a hallmark of hippocampal activity across mammals and play a critical role in many hippocampal models of memory and spatial navigation. To reconcile the cross-species differences observed in the presence and properties of theta, we recorded hippocampal local field potentials in rats and ferrets during auditory and visual localisation tasks designed to vary locomotion and sensory attention. Here, we show that theta oscillations occur during locomotion in both ferrets and rats, however during periods of immobility, theta oscillations persist in the ferret, contrasting starkly with the switch to large irregular activity (LIA) in the rat. Theta during immobility in the ferret is identified as analogous to Type 2 theta that has been observed in rodents due to its sensitivity to atropine, and is modulated by behavioural state with the strongest theta observed during reward epochs. These results demonstrate that even under similar behavioural conditions, differences exist between species in the relationship between theta and behavioural state.

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Classical work in rodents demonstrated two mechanistically distinct types of theta oscillations: fast Type-1 (atropine-insensitive) theta oscillations (7-11 Hz) during locomotion, and slower Type-2 (atropine-sensitive) oscillations (4-7 Hz) thought to occur preferentially during immobility.
“Classical work in rodents has demonstrated the existence of two mechanistically distinct types of theta oscillations: fast Type-1 (atropine-insensitive) theta oscillations (7–11 Hz), which are observed during locomotion, and slower Type-2 (atropine-sensitive) oscillations (4–7 Hz), which are thought to preferentially occur during immobility26–28,42,50,97.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [50]
The Introduction (page unavailable) describes two types of rat theta with distinct behavioural correlates and pharmacology: atropine-resistant Type 1 during locomotion and atropine-sensitive Type 2 during immobility at 4–7 Hz. It says Type 1 is faster than Type 2, but does not give the claimed 7–11 Hz range for Type 1 or explicitly establish that the two rodent types arise from distinct mechanisms. (LLM, conf=0.85)
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Fitting Linear Mixed-Effects Models Using lme4
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015) · Journal of Statistical Software · doi:10.18637/jss.v067.i01 · Cited by 86,835 · see citing works
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151 · see citing works
Computer visualization of three-dimensional image data using IMOD.
Kremer, J. R., Mastronarde, D., & Mcintosh, J. (1996) · Journal of Structural Biology · doi:10.1006/jsbi.1996.0013 · Cited by 5,770 · see citing works
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
CircStat : A MATLAB Toolbox for Circular Statistics
Berens, P. (2009) · Journal of Statistical Software · doi:10.18637/jss.v031.i10 · Cited by 3,099 · see citing works
Phase relationship between hippocampal place units and the EEG theta rhythm
O'Keefe, J. M., & Recce, M. L. (1993) · Hippocampus · doi:10.1002/hipo.450030307 · Cited by 2,561 · see citing works
Hippocampal electrical activity and voluntary movement in the rat
Vanderwolf, C. H. (1969) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(69)90092-3 · Cited by 1,928 · see citing works
Memory, navigation and theta rhythm in the hippocampal-entorhinal system
Buzsáki, G., & Moser, E. I. (2013) · Nature Neuroscience · doi:10.1038/nn.3304 · Cited by 1,847 · see citing works
Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis
Taube, J., Muller, R., & Ranck, J. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00420.1990 · Cited by 1,809 · see citing works
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
The theta-gamma neural code
Lisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · see citing works
Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat
Bragin, A., Jando, G., Nadasdy, Z., Hetke, J., Wise, K., & Buzsaki, G. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00047.1995 · Cited by 1,527 · see citing works
HIPPOCAMPAL ELECTRICAL ACTIVITY IN AROUSAL
Green, J. D., & Arduini, A. (1954) · Journal of Neurophysiology · doi:10.1152/jn.1954.17.6.533 · Cited by 1,392 · see citing works
Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo
Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003) · Nature · doi:10.1038/nature01374 · Cited by 1,345 · see citing works
The physiology and pharmacology of hippocampal formation theta rhythms
Bland, B. H. (1986) · Progress in Neurobiology · doi:10.1016/0301-0082(86)90019-5 · Cited by 1,039 · see citing works
Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task
Jones, M. W., & Wilson, M. A. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030402 · Cited by 1,036 · see citing works
Prefrontal phase locking to hippocampal theta oscillations
Siapas, A. G., Lubenov, E. V., & Wilson, M. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.028 · Cited by 1,014 · see citing works
Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms
Buzsáki, G., Logothetis, N., & Singer, W. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.002 · Cited by 886 · see citing works
A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning
Hasselmo, M. E., Bodelón, C., & Wyble, B. P. (2002) · Neural Computation · doi:10.1162/089976602317318965 · Cited by 875 · see citing works
Loss of Hippocampal Theta Rhythm Results in Spatial Memory Deficit in the Rat
Winson, J. (1978) · Science · doi:10.1126/science.663646 · Cited by 857 · see citing works
Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: Relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital
Kramis, R., Vanderwolf, C. H., & Bland, B. H. (1975) · Experimental Neurology · doi:10.1016/0014-4886(75)90195-8 · Cited by 791 · see citing works
Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus
Belluscio, M. A., Mizuseki, K., Schmidt, R., Kempter, R., & Buzsáki, G. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4122-11.2012 · Cited by 784 · see citing works
Amygdalar and Hippocampal Theta Rhythm Synchronization During Fear Memory Retrieval
Seidenbecher, T., Laxmi, T. R., Stork, O., & Pape, H.-C. (2003) · Science · doi:10.1126/science.1085818 · Cited by 728 · see citing works
Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop
Mizuseki, K., Sirota, A., Pastalkova, E., & Buzsáki, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.037 · Cited by 718 · see citing works
Hippocampal electrical activity during the development of conditioned reflexes
Grastyán, E., Lissák, K., Madarász, I., & Donhoffer, H. (1959) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(59)90040-9 · Cited by 585 · see citing works
Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II
Alonso, Á., & Llinás, R. R. (1989) · Nature · doi:10.1038/342175a0 · Cited by 568 · see citing works
Mechanisms and functions of theta rhythms
Colgin, L. L. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170330 · Cited by 559 · see citing works
Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration
Bland, B. H., & Oddie, S. D. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00358-8 · Cited by 520 · see citing works
Biology and Diseases of the Ferret
(2014) · Wiley eBooks · doi:10.1002/9781118782699 · Cited by 512 · see citing works
Hippocampal EEG and behavior: Change in amplitude and frequency of RSA (Theta rhythm) associated with spontaneous and learned movement patterns in rats and cats
Whishaw, I. Q., & Vanderwolf, C. H. (1973) · Behavioral Biology · doi:10.1016/s0091-6773(73)80041-0 · Cited by 508 · see citing works
Representation of Three-Dimensional Space in the Hippocampus of Flying Bats
Yartsev, M. M., & Ulanovsky, N. (2013) · Science · doi:10.1126/science.1235338 · Cited by 403 · see citing works
Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats
Mitchell, S., Rawlins, J. N. P., Steward, O., & Olton, D. S. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-03-00292.1982 · Cited by 401 · see citing works
Grid cells without theta oscillations in the entorhinal cortex of bats
Yartsev, M. M., Witter, M. P., & Ulanovsky, N. (2011) · Nature · doi:10.1038/nature10583 · Cited by 391 · see citing works
Gamma Oscillations in the Hippocampus
Colgin, L. L., & Moser, E. I. (2010) · Physiology · doi:10.1152/physiol.00021.2010 · Cited by 376 · see citing works
Theta-paced flickering between place-cell maps in the hippocampus
Jezek, K., Henriksen, E. J., Treves, A., Moser, E. I., & Moser, M.-B. (2011) · Nature · doi:10.1038/nature10439 · Cited by 359 · see citing works
Using Grid Cells for Navigation
Bush, D., Barry, C., Manson, D., & Burgess, N. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.006 · Cited by 334 · see citing works
Theta sequences are essential for internally generated hippocampal firing fields
Wang, Y., Romani, S., Lustig, B. R., Leonardo, A. M., & Pastalkova, E. (2014) · Nature Neuroscience · doi:10.1038/nn.3904 · Cited by 314 · see citing works
Self-generated theta oscillations in the hippocampus
Goutagny, R., Jackson, J., & Williams, S. (2009) · Nature Neuroscience · doi:10.1038/nn.2440 · Cited by 301 · see citing works
Constant Sub-second Cycling between Representations of Possible Futures in the Hippocampus
Kay, K., Chung, J. E., Sosa, M., Schor, J. S., Karlsson, M. P., Larkin, M. C., Liu, D. F., & Frank, L. M. (2020) · Cell · doi:10.1016/j.cell.2020.01.014 · Cited by 296 · see citing works
Hippocampal cellular and network activity in freely moving echolocating bats
Ulanovsky, N., & Moss, C. F. (2007) · Nature Neuroscience · doi:10.1038/nn1829 · Cited by 283 · see citing works
Oscillatory activity in the monkey hippocampus during visual exploration and memory formation
Jutras, M. J., Fries, P., & Buffalo, E. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1302351110 · Cited by 274 · see citing works
Theta rhythm and the encoding and retrieval of space and time
Hasselmo, M. E., & Stern, C. E. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.022 · Cited by 261 · see citing works
Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory
Jacobs, J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0304 · Cited by 259 · see citing works
Restoring theta‐like rhythmicity in rats restores initial learning in the Morris water maze
McNaughton, N., Ruan, M., & Woodnorth, M. (2006) · Hippocampus · doi:10.1002/hipo.20235 · Cited by 255 · see citing works
Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: Current-source density analysis, effects of urethane and atropine
Buzsáki, G., Czopf, J., Kondákor, I., & Kellényi, L. (1986) · Brain Research · doi:10.1016/0006-8993(86)90729-8 · Cited by 250 · see citing works
Relationship between hippocampal theta activity and running speed in the rat.
McFarland, W. L., Teitelbaum, H., & Hedges, E. K. (1975) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0076177 · Cited by 237 · see citing works
Hippocampus, theta, and spatial memory
O'Keefe, J. M. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90163-s · Cited by 226 · see citing works
Cycle-by-cycle analysis of neural oscillations
Cole, S. R., & Voytek, B. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00273.2019 · Cited by 225 · see citing works
Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation
Bohbot, V. D., Copara, M. S., Gotman, J., & Ekstrom, A. D. (2017) · Nature Communications · doi:10.1038/ncomms14415 · Cited by 217 · see citing works
Functionally distinct high and low theta oscillations in the human hippocampus
Goyal, A., Miller, J. F., Qasim, S. E., Watrous, A. J., Zhang, H., Stein, J. M., Inman, C. S., Gross, R. E., Willie, J. T., Lega, B. C., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15670-6 · Cited by 215 · see citing works
The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion
Sławińska, U., & Kasicki, S. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00390-4 · Cited by 201 · see citing works
Hippocampal rhythmic slow activity (RSA, theta): A critical analysis of selected studies and discussion of possible species-differences
Robinson, T. E. (1980) · Brain Research Reviews · doi:10.1016/0165-0173(80)90004-1 · Cited by 197 · see citing works
Behavior-Dependent Coordination of Multiple Theta Dipoles in the Hippocampus
Montgomery, S. M., Betancur, M. I., & Buzsáki, G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4339-08.2009 · Cited by 190 · see citing works
Theta Oscillations in the Human Medial Temporal Lobe during Real-World Ambulatory Movement
M. Aghajan, Z., Schuette, P., Fields, T. A., Tran, M. E., Siddiqui, S. M., Hasulak, N. R., Tcheng, T. K., Eliashiv, D., Mankin, E. A., Stern, J., et al. (2017) · Current Biology · doi:10.1016/j.cub.2017.10.062 · Cited by 186 · see citing works
Differences in subthreshold resonance of hippocampal pyramidal cells and interneurons: the role of h‐current and passive membrane characteristics
Zemankovics, R., Káli, S., Paulsen, O., Freund, T. F., & Hájos, N. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2009.185975 · Cited by 183 · see citing works
Organization of primary visual cortex (area 17) in the ferret
Law, M. I., Zahs, K. R., & Stryker, M. P. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902780202 · Cited by 175 · see citing works
Hippocampal Respiration-Driven Rhythm Distinct from Theta Oscillations in Awake Mice
Nguyen Chi, V., Müller, C., Wolfenstetter, T., Yanovsky, Y., Draguhn, A., Tort, A. B. L., & Brankačk, J. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2848-15.2016 · Cited by 171 · see citing works
Behavioral correlates of hippocampal type 2 theta in the rat
Sainsbury, R. S., Heynen, A., & Montoya, C. P. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90382-9 · Cited by 168 · see citing works
Electrical stimulation of the brain stem in freely moving rats: II. Effects on hippocampal and neocortical electrical activity, and relations to behavior
Robinson, T. E., & Vanderwolf, C. H. (1978) · Experimental Neurology · doi:10.1016/0014-4886(78)90018-3 · Cited by 168 · see citing works
A comparative study of human and rat hippocampal low‐frequency oscillations during spatial navigation
Watrous, A. J., Lee, D. J., Izadi, A., Gurkoff, G. G., Shahlaie, K., & Ekstrom, A. D. (2013) · Hippocampus · doi:10.1002/hipo.22124 · Cited by 163 · see citing works
A Respiration-Coupled Rhythm in the Rat Hippocampus Independent of Theta and Slow Oscillations
Lockmann, A. L. V., Laplagne, D. A., Leão, R. N., & Tort, A. B. L. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3452-15.2016 · Cited by 152 · see citing works
Theta Phase Modulates Multiple Layer-Specific Oscillations in the CA1 Region
Scheffer-Teixeira, R., Belchior, H., Caixeta, F. V., Souza, B. C., Ribeiro, S. T. G., & Tort, A. B. L. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr319 · Cited by 138 · see citing works
Frequency of theta rhythm is controlled by acceleration, but not speed, in running rats
Kropff, E., Carmichael, J. E., Moser, E. I., & Moser, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.01.017 · Cited by 125 · see citing works
Comparative anatomy of the entorhinal cortex and hippocampus in mammals
Insausti, R. (1993) · Hippocampus · doi:10.1002/hipo.1993.4500030705 · Cited by 114 · see citing works
Ventral hippocampal OLM cells control type 2 theta oscillations and response to predator odor
Mikulovic, S., Restrepo, C. E., Siwani, S., Bauer, P., Pupe, S., Tort, A. B. L., Kullander, K., & Leão, R. N. (2018) · Nature Communications · doi:10.1038/s41467-018-05907-w · Cited by 114 · see citing works
Human hippocampal theta power indicates movement onset and distance travelled
Bush, D., Bisby, J. A., Bird, C. M., Gollwitzer, S., Rodionov, R., Diehl, B., McEvoy, A. W., Walker, M. C., & Burgess, N. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708716114 · Cited by 112 · see citing works
Hippocampal electroencephalographic activity in the Mongolian gerbil during natural behaviors and wheel running and in the rat during wheel running and conditioned immobility.
Whishaw, I. Q. (1972) · Canadian Journal of Psychology/Revue Canadienne de Psychologie · doi:10.1037/h0082431 · Cited by 111 · see citing works
The relationship between type 2 theta and behavior
Sainsbury, R. S., & Montoya, C. P. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90381-0 · Cited by 111 · see citing works
Hippocampal theta activity in monkeys
Stewart, M., & Fox, S. E. (1991) · Brain Research · doi:10.1016/0006-8993(91)90376-7 · Cited by 110 · see citing works
Spectral analysis of hippocampal EEG in the freely moving rat: Effects of centrally active drugs and relations to evoked potentials
Leung, L.-W. S. (1985) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(85)90952-6 · Cited by 106 · see citing works
Nonoscillatory Phase Coding and Synchronization in the Bat Hippocampal Formation
Eliav, T., Geva-Sagiv, M., Yartsev, M. M., Finkelstein, A., Rubin, A., Las, L., & Ulanovsky, N. (2018) · Cell · doi:10.1016/j.cell.2018.09.017 · Cited by 106 · see citing works
Dogs Have the Most Neurons, Though Not the Largest Brain: Trade-Off between Body Mass and Number of Neurons in the Cerebral Cortex of Large Carnivoran Species
Jardim-Messeder, D., Lambert, K. G., Noctor, S. C., Pestana, F. M., Leal, M. E. D. C., Bertelsen, M. F., Alagaili, A. N., Mohammad, O. B., Manger, P. R., & Herculano‐Houzel, S. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00118 · Cited by 103 · see citing works
Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination
Grion, N., Akrami, A., Zuo, Y., Stella, F., & Diamond, M. E. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002384 · Cited by 89 · see citing works
Effects of medial and lateral septal lesions on acquisition of a place and cue radial maze task
M'Harzi, M., & Jarrard, L. E. (1992) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80160-3 · Cited by 87 · see citing works
Spatial encoding in primate hippocampus during free navigation
Courellis, H. S., Nummela, S. U., Metke, M., Diehl, G. W., Bussell, R., Cauwenberghs, G., & Miller, C. T. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000546 · Cited by 84 · see citing works
The acoustical cues to sound location in the rat: Measurements of directional transfer functions
Koka, K., Read, H. L., & Tollin, D. J. (2008) · The Journal of the Acoustical Society of America · doi:10.1121/1.2916587 · Cited by 81 · see citing works
Hippocampal EEG and behaviour in dog. I. Hippocampal EEG correlates of gross motor behaviour
Arnolds, D. E. A. T., Lopes, F. H. D. S., Aitink, J. W., & Kamp, A. (1979) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(79)90009-9 · Cited by 72 · see citing works
Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks
López‐Madrona, V. J., Pérez-Montoyo, E., Álvarez-Salvado, E., Moratal, D., Herreras, Ó., Pereda, E., Mirasso, C. R., & Canals, S. (2020) · eLife · doi:10.7554/elife.57313 · Cited by 72 · see citing works
Arousal dependent modulation of thalamo-cortical functional interaction
Stitt, I., Zhou, Z. C., Radtke‐Schuller, S., & Frӧhlich, F. (2018) · Nature Communications · doi:10.1038/s41467-018-04785-6 · Cited by 70 · see citing works
Movement Enhances the Nonlinearity of Hippocampal Theta
Sheremet, A., Burke, S. N., & Maurer, A. P. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3564-15.2016 · Cited by 64 · see citing works
Hippocampal EEG and behaviour in dog. II. Hippocampal EEG correlates with elementary motor acts
Arnolds, D. E. A. T., da Silva, F. H. L., Aitink, J. W., et al. (1979) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(79)90010-5 · Cited by 59 · see citing works
Hippocampal theta rhythm persists in the permanently isolated forebrain of the cat
Olmstead, C. E., & Villablanca, J. R. (1977) · Brain Research Bulletin · doi:10.1016/0361-9230(77)90004-1 · Cited by 55 · see citing works
Cyto- and Myeloarchitectural Brain Atlas of the Ferret (Mustela putorius) in MRI Aided Stereotaxic Coordinates
Radtke‐Schuller, S. (2018) · Springer eBooks · doi:10.1007/978-3-319-76626-3 · Cited by 52 · see citing works
Hippocampal EEG and behaviour in dog. III. Hippocampal EEG correlates of stimulus-response tasks and of sexual behaviour
Arnolds, D. E. A. T., da Silva, F. H. L., Aitink, J. W., et al. (1979) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(79)90011-7 · Cited by 40 · see citing works
Midline and lateral field sound localization in the albino rat (Rattus norvegicus).
Kavanagh, G. L., & Kelly, J. B. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.2.200 · Cited by 39 · see citing works
Midline and lateral field sound localization in the albino rat (Rattus norvegicus).
Kavanagh, G. L., & Kelly, J. B. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.200 · Cited by 37 · see citing works
The quantitative effect of visual and tactile stimuli on the prey-catching behaviour of ferrets (Putorius furo L.)
Apfelbach, R., & Wester, U. (1977) · Behavioural Processes · doi:10.1016/0376-6357(77)90020-1 · Cited by 35 · see citing works
Neurons in primary auditory cortex represent sound source location in a cue-invariant manner
Wood, K. C., Town, S. M., & Bizley, J. K. (2019) · Nature Communications · doi:10.1038/s41467-019-10868-9 · Cited by 34 · see citing works
Self-citation
Hearing in the ferret (Mustela putorius): effects of primary auditory cortical lesions on thresholds for pure tone detection
Kavanagh, G. L., & Kelly, J. B. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.60.3.879 · Cited by 32 · see citing works
Behavioural sensitivity to binaural spatial cues in ferrets: evidence for plasticity in the duplex theory of sound localization
Keating, P., Nodal, F. R., & King, A. J. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12402 · Cited by 30 · see citing works
Hippocampal and cortical activity during sexual behavior in the female rat.
Kurtz, R. G. (1975) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0076650 · Cited by 29 · see citing works
Hippocampal theta rhythms follow the beat of their own drum
Colgin, L. L., & Moser, E. I. (2009) · Nature Neuroscience · doi:10.1038/nn1209-1483 · Cited by 28 · see citing works
Macroscopic and roentgenographic anatomy of the skull of the ferret ( Mustela putorius furo )
He, T., Friede, H., & Kiliaridis, S. (2002) · Laboratory Animals · doi:10.1258/0023677021911795 · Cited by 25 · see citing works
Modality specific Type 2 theta production in the immobile rat.
Montoya, C. P., Heynen, A. J., Faris, P. D., & Sainsbury, R. S. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.1.106 · Cited by 24 · see citing works
Regional distribution of cholinergic, catecholaminergic, serotonergic and orexinergic neurons in the brain of two carnivore species: The feliform banded mongoose ( Mungos mungo ) and the caniform domestic ferret ( Mustela putorius furo )
Pillay, S., Bhagwandin, A., Bertelsen, M. F., Patzke, N., Engler, G., Engel, A. K., & Manger, P. R. (2017) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2017.04.001 · Cited by 21 · see citing works
Visual Motion and Form Integration in the Behaving Ferret
Dunn-Weiss, E., Nummela, S. U., Lempel, A. A., Law, J. M., Ledley, J., Salvino, P., & Nielsen, K. J. (2019) · eNeuro · doi:10.1523/eneuro.0228-19.2019 · Cited by 16 · see citing works
Optokinetic nystagmus in the ferret: including selected comparisons with the cat
Hein, A., Courjon, J. H., Flandrin, J. M., et al. (1990) · Experimental Brain Research · doi:10.1007/bf00229330 · Cited by 15 · see citing works
Initiation of sleep-dependent cortical-hippocampal correlations at wakefulness-sleep transition.
Haggerty, D., & Ji, D.-Y. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00783.2013 · Cited by 10 · see citing works
Movement-dependent and movement-independent changes in hippocampal RSA in cats
Frederickson, C. J., Smylie, C. S., Howell, G. A., & Lenig, R. B. (1978) · Brain Research Bulletin · doi:10.1016/0361-9230(78)90087-4 · Cited by 10 · see citing works
Sex differences and effects of the estrous stage on hippocampal‐prefrontal theta communications
Schoepfer, K. J., Xu, Y., Wilber, A. A., Wu, W., & Kabbaj, M. (2020) · Physiological Reports · doi:10.14814/phy2.14646 · Cited by 10 · see citing works
The hippocampal formation of two carnivore species: The feliform banded mongoose and the caniform domestic ferret
Pillay, S., Bhagwandin, A., Bertelsen, M. F., Patzke, N., Engler, G., Engel, A. K., & Manger, P. R. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.25047 · Cited by 7 · see citing works
Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility - data
Dunn, S., Town, S., Bizley, J., et al. (2022) · Figshare · doi:10.5522/04/21070128 · Cited by 1 · see citing works
Self-citation
Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility - figures
Dunn, S., Town, S., Bizley, J., et al. (2022) · University College London · doi:10.5522/04/20809099 · Cited by 1 · see citing works
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Research works printed but not linked: 1

[107]Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates. (Elsevier Academic Press, 2005).

Sorted by citations

Place and behavioral modulation of hippocampal neurons during immobility
Sartorato, N., Zouridis, I. S., Narantsatsralt, U.-U., Blanco-Hernández, E., & Burgalossi, A. (2026) · Nature Communications · doi:10.1038/s41467-026-75492-w · Cited by 1 · see citing works

Effects of subtotal hippocampal lesions upon hippocampal electrical activity
Helmes, E., & Vanderwolf, C. H. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90143-8 · Cited by 3 · see citing works
Radioautographic analysis of [14C]2-deoxyglucose uptake in hippocampal formation of the rat during enforced locomotor activity-induced theta
Monmaur, P., Orsini, J. C., & Delacour, J. (1982) · Brain Research · doi:10.1016/0006-8993(82)91138-6 · Cited by 6 · see citing works
Frequency‐ and state‐dependent effects of hippocampal neural disinhibition on hippocampal local field potential oscillations in anesthetized rats
Gwilt, M., Bauer, M., & Bast, T. (2020) · Hippocampus · doi:10.1002/hipo.23212 · Cited by 9 · see citing works
Comparison of the effect of β-amyloid peptide 25-35 on hippocampal and septal neurons in vitroi
Zhao, Y. (2004)
Role of long-range projecting inhibitory neurons in hippocampal network oscillations
Tamburri, A. (2013) · University of Birmingham Institutional Research Archive (University of Birmingham)

Authors: Dunn, S. L. S., Town, S. M., Bizley, J. K., & Bendor, D.
Affiliations: University College London (GB)
Corresponding author: Dunn, Soraya L. S.
ORCID: Dunn, Soraya L. S.
Town, Stephen M.
Bizley, Jennifer K.
Bendor, Daniel
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2022-10-07
Volume: 13
Issue: 1
Pages: 5905-5905
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/s41467-022-33507-2
PMC: PMC9547075
OpenAlex: W4303022253
Cited by: 17
References: 104
Citations by year: 2026: 3 · 2025: 4 · 2024: 3 · 2023: 5 · 2022: 2
FWCI: 1.81
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Wellcome Trust (098418/Z/12/Z)
Biotechnology and Biological Sciences Research Council (BB/R004420/1)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: hippocampal theta oscillations, behavioral state, locomotion, immobility, atropine sensitivity, sound localization, visual localization, reward, rats, ferrets, local field potentials
MeSH terms: Animals, Atropine, Ferrets, Hippocampus, Locomotion, Theta Rhythm, Rats

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Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility

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