Oscillatory Entrainment of Thalamic Neurons by Theta Rhythm in Freely Moving Rats

Tsanov, Marian; Chah, Ehsan; Wright, Nicholas Fraser; Vann, Seralynne Denise; Reilly, Richard B.; Erichsen, Jonathan Thor; Aggleton, John Patrick; O’Mara, Shane M.

doi:10.1152/jn.00771.2010

Cited by 49 publications

(60 citation statements)

References 81 publications

(78 reference statements)

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“…4) were inhibitory neurons (Ranck, 1973;Freund and Antal, 1988), whereas theta cells in the anterior thalamus (Fig. 2) may have been excitatory thalamocortical projection neurons (Jones, 1985;Tsanov et al, 2011b). We thus conducted simulations to test whether spatial tuning functions could be formed by inhibitory versus excitatory inputs to a postsynaptic target neuron from theta cells.…”

Section: Place Cell Synthesized From Theta Cells On a Linear Trackmentioning

confidence: 99%

Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference

et al. 2011

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Section: Place Cell Synthesized From Theta Cells On a Linear Trackmentioning

confidence: 99%

Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference

et al. 2011

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“…potentials measured with such electrodes have been recently shown to reflect to the theta oscillatory activity of single theta cells in anterior thalamus (Tsanov et al, 2011a). Once verification of the location of the electrodes was complete, recordings were allowed to stabilize for 10 min prior to the experiment.…”

Section: Electrophysiological Experiments Surgical Preparationmentioning

confidence: 99%

Hippocampal inputs mediate theta-related plasticity in anterior thalamus

et al. 2011

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Hippocampally-driven oscillatory activity at theta frequency is found in the diencephalon, but an understanding of the fundamental role of theta in the hippocampo-diencephalic circuit remains elusive. An important strategy in determining how activity modifies oscillatory properties of hippocampo-diencephalic circuitry comprises investigations of anterior thalamic responses to their main inputs: the descending dorsal fornix and the ascending mammillothalamic tract. Here, we show that the amplitude of thalamic theta spectral power selectively increases after plasticityinducing stimulation of the dorsal fornix, but not of the mammillothalamic tract in urethaneanaesthetized young male rats. Furthermore, we show that low-frequency stimulation (LFS) significantly augments the fornix-driven theta ratio (theta over delta power, T-ratio), in parallel with depressing thalamic synaptic responses. However, the mammillothalamic synaptic response after LFS did not correlate with the slow band of theta oscillation (low T-ratio), but did correlate positively with the fast band of theta oscillation (high T-ratio). Our data demonstrate that the descending direct fornix projection is a pathway that modulates theta rhythm in the hippocampodiencephalic circuit, resulting in dynamic augmentation of thalamic neuronal responsiveness. These findings suggest that hippocampal theta differentially affects synaptic integration in the different structures with which the hippocampus is reciprocally connected. Keywordsanterior thalamic nuclei; fornix; mammillothalamic tract; synaptic plasticity; theta oscillation; LTP The functioning of the thalamus and the hippocampus cannot be fully elucidated without considering them as a unified network (Steriade, 2001;Warburton et al., 2001). In this context, hippocampal oscillations would be expected to have an impact on the neuronal activity of the anterior thalamic nuclei (ATN) but how the signals are actually processed through the hippocampo-diencephalic loop remains poorly understood. Large neuronal populations in ATN oscillate with frequency of 6-11 Hz, in the range of theta rhythm (Vertes et al., 2001;Tsanov et al., 2011a). Theta oscillations are a characteristic feature also of the main regions providing anterior thalamic inputs: the hippocampal formation and the medial mammillary bodies, that is the "medial" hippocampo-diencephalic system Theta rhythm has been especially related to the processes of episodic memory formation in the extended hippocampal system (Buzsáki, 2005). The hippocampus receives two main types of input: the first one is the theta input from the medial septum, which reverberates through hippocampo-diencephalic loop (Fig. 1A). The second hippocampal input is a highly-processed sensory information originating from multiple neocortical regions. The temporal convergence of activity from neocortical and diencephalic inputs would result in long-term storage of the encoded information. Because theta activity induces a fluctuation in cellular excitability, the probability tha...

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“…Concurrently, the thalamic theta signal may also integrate septal theta oscillations and idiothetic signals. Anteroventral thalamic neurons, which express thetabursting and theta-modulated properties (Tsanov et al, 2011b;Vertes et al, 2001), have recently been shown to encode directional signals (Tsanov et al, 2011a). This study identified a population of anteroventral theta-bursting cells that undergo directional modulation of their spiking in the horizontal plane (Fig.…”

mentioning

confidence: 99%

“…In the Papez's circuit, linear velocity is integrated by the oscillatory and spiking patterns of the medial mammillary bodies (Sharp and Turner-Williams, 2005). Neuronal populations that oscillate at theta frequency are also found in the anteroventral thalamic nucleus, a functional-anatomical interface between thalamic oscillatory activity, and limbic theta activity during vigilant behaviour (Tsanov et al, 2011b;Vertes et al, 2001). Our recent preliminary work found that theta periods express a higher peak firing rate for the preferred firing direction of heading, compared to the peak firing rate during non-theta periods (Tsanov et al, 2011c).…”

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Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

Tsanov

O’Mara

2015

Brain Research

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a b s t r a c tA major tool in understanding how information is processed in the brain is the analysis of neuronal output at each hierarchical level through which neurophysiological signals are propagated. Since the experimental brain operation performed on Henry Gustav Molaison (known as patient H.M.) in 1953, the hippocampal formation has gained special attention, resulting in a very large number of studies investigating signals processed by the hippocampal formation. One of the main information streams to the hippocampal formation, vital for episodic memory formation, arises from thalamo-hippocampal projections, as there is extensive connectivity between these structures. This connectivity is sometimes overlooked by theories of memory formation by the brain, in favour of theories with a strong corticohippocampal flavour. In this review, we attempt to address some of the complexity of the signals processed within the thalamo-hippocampal circuitry. To understand the signals encoded by the anterior thalamic nuclei in particular, we review key findings from electrophysiological, anatomical, behavioural and computational studies. We include recent findings elucidating the integration of different signal modalities by single thalamic neurons;we focus in particular on the propagation of two prominent signals: head directionality and theta rhythm. We conclude that thalamo-hippocampal processing provides a centrally important, substantive, and dynamic input modulating and moderating hippocampal spatial and mnemonic processing. This article is part of a Special Issue entitled SI: Brain and Memory.& 2014 Published by Elsevier B.V. IntroductionThe purpose of the present review is to dissect some of the complexity of the signals propagated from anterior thalamus to the hippocampal formation in order to try and understand the importance of this information processing for the coding properties of individual neurons in the hippocampus. "Anterior thalamus" includes the anterodorsal, anteroventral and dorsolateral thalamic nuclei, which form the thalamic component of the limbic system (the 'thalamic

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Oscillatory Entrainment of Thalamic Neurons by Theta Rhythm in Freely Moving Rats

Cited by 49 publications

References 81 publications

Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference

Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference

Hippocampal inputs mediate theta-related plasticity in anterior thalamus

Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

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