Multiplexed oscillations and phase rate coding in the basal forebrain

Tingley, David; Alexander, Andrew S.; Quinn, Laleh K.; Chiba, Andrea A.; Nitz, Douglas A.

doi:10.1126/sciadv.aar3230

Cited by 35 publications

(35 citation statements)

References 68 publications

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“…This could play a mitigating role in amplifying the amplitude relationship between septal output frequency to the hippocampus and local theta oscillations. However, the reciprocal influence of the hippocampus to the MS via the lateral septum cannot be excluded (Tingley, Alexander, Quinn, Chiba, & Nitz, 2018).…”

Section: Discussionmentioning

confidence: 99%

Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

et al. 2020

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Hippocampal theta oscillations show prominent changes in frequency and amplitude depending on behavioral state or cognitive demands. How these dynamic changes in theta oscillations contribute to the spatial and temporal organization of hippocampal cells, and ultimately behavior, remain unclear. We used low-theta frequency optogenetic stimulation to pace coordination of cellular and network activity between the medial septum (MS) and hippocampus during baseline and MS stimulation while rats were at rest or performing a spatial accuracy task with a visible or hidden goal zone. Hippocampal receptivity to pan-neuronal septal stimulation at low-theta frequency was primarily determined by speed and secondarily by task demands. Competition between artificial and endogenous field potentials at theta frequency attenuated hippocampal phase preference relative to local theta, but the spike-timing activity of hippocampal pyramidal cells was effectively driven by artificial septal output, particularly during the hidden goal task. Notwithstanding temporal reorganization by artificial theta stimulation, place field properties were unchanged and alterations to spatial behavior were limited to goal zone approximation. Our results indicate that even a low-theta frequency timing signal in the septohippocampal circuit is sufficient for spatial goal finding behavior. The results also advance a mechanistic understanding of how endogenous or artificial somatodendritic timing signals relate to displacement computations during navigation and spatial memory.

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Section: Discussionmentioning

confidence: 99%

Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

et al. 2020

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“…Phase precession has predominantly been observed during place-or grid-cell spiking 67 . However, recent work has discovered the presence of phase precession relative to sound 33,34 , odor 34 , time in an episode [29][30][31] , task progression 27 , and REM sleep 29 . These findings highlight the potential generalizability of phase precession to non-spatial domains.…”

Section: Discussionmentioning

confidence: 99%

“…While phase precession is often described in hippocampal place cells or entorhinal grid cells, it has also been observed in a diverse range of brain areas such as ventral striatum 25 , subiculum 26 , basal forebrain 27 , and medial prefrontal cortex 28 . Critically, a slew of recent work has directly observed phase precession independent of location within a place or grid field, encoding elapsed time during REM sleep 29 , wheel-running 30 , jumping 31 , fixation 32 , presentation of task-relevant stimuli [33][34][35] , and task epoch 27 . The widespread prevalence of phase precession suggests that this phenomenon has a more general role beyond representing the current spatial location, and that it could be relevant for building neural representations in many regions to support diverse aspects of cognition, learning, and memory.…”

Section: Introductionmentioning

confidence: 99%

“…Evidence for phase precession without spatial coding. While phase precession has been observed most readily relative to specific spatial locations, there is also evidence for precession with respect to non-spatial behaviors and stimuli 27,[29][30][31]33 , and in regions outside the hippocampal formation 25,28 . These findings suggest that phase precession could be a more general phenomenon that the brain uses to represent diverse types of consecutive, relevant stimuli/states using different phases of an oscillation.…”

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Phase precession in the human hippocampus and entorhinal cortex

Qasim

Fried

Jacobs

2020

Preprint

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Knowing where we are, where we have been, and where we are going is critical to many behaviors, including navigation and memory. One potential neuronal mechanism underlying this ability is phase precession, in which spatially tuned neurons represent sequences of positions by activating at progressively earlier phases of local network theta (~5-10~Hz) oscillations. Phase precession may be a general neural pattern for representing sequential events for learning and memory. However, phase precession has never been observed in humans. By recording human single-neuron activity during spatial navigation, we show that spatially tuned neurons in the human hippocampus and entorhinal cortex exhibit phase precession. Furthermore, beyond the neural representation of locations, we show evidence for phase precession related to specific goal-states. Our findings thus extend theta phase precession to humans and suggest that this phenomenon has a broad functional role for the neural representation of both spatial and non-spatial information.

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“…Local Field Potentials (LFP) primarily represent summed transmembrane currents in the vicinity of an electrode and reflect neuronal ensemble activity (Ahmed and Cash, 2013;Buzsáki et al, 2012;Destexhe et al, 1999;Einevoll et al, 2013;Gold et al, 2006;Kajikawa and Schroeder, 2011;Katzner et al, 2009;Kelly et al, 2010;Telenczuk et al, 2017;Tingley et al, 2018). The information carried by LFPs is typically deciphered using frequency domain techniques that require averaging over several oscillatory cycles.…”

Section: Introductionmentioning

confidence: 99%

Instantaneous amplitude and shape of postrhinal theta oscillations differentially encode running speed

Ghosh

Shanahan

Furtak

et al. 2020

Preprint

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Hippocampal theta oscillations have a temporally asymmetric waveform shape, but it is not known if this theta asymmetry extends to all other cortical regions involved in spatial navigation and memory. Here, using both established and improved cycle-by-cycle analysis methods, we show that theta waveforms in the postrhinal cortex are also temporally asymmetric. On average, the falling phase of postrhinal theta cycles lasts longer than the subsequent rising phase. There are, however, rapid changes in both the instantaneous amplitude and instantaneous temporal asymmetry of postrhinal theta cycles. These rapid changes in amplitude and asymmetry are very poorly correlated, indicative of a mechanistic disconnect between these theta cycle features. We show that the instantaneous amplitude and asymmetry of postrhinal theta cycles differentially encode running speed. Although theta amplitude continues to increase at the fastest running speeds, temporal asymmetry of the theta waveform shape plateaus after medium speeds. Our results suggest that the amplitude and waveform shape of individual postrhinal theta cycles may be governed by partially independent mechanisms and emphasize the importance of employing a single cycle approach to understanding the genesis and behavioral correlates of cortical theta rhythms.

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Multiplexed oscillations and phase rate coding in the basal forebrain

Abstract: Basal forebrain transforms multiplexed oscillatory inputs into a phase rate–coded output of task phase during complex behavior.

Cited by 35 publications

References 68 publications

Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

Optogenetic “low‐theta” pacing of the septohippocampal circuit is sufficient for spatial goal finding and is influenced by behavioral state and cognitive demand

Phase precession in the human hippocampus and entorhinal cortex

Instantaneous amplitude and shape of postrhinal theta oscillations differentially encode running speed

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