Effects of visual inputs on neural dynamics for coding of location and running speed in medial entorhinal cortex

Dannenberg, Heinz; Lazaro, Hallie; Nambiar, Pranav; Hoyland, Alec; Hasselmo, Michael E.

doi:10.7554/elife.62500

Cited by 30 publications

(42 citation statements)

References 89 publications

(174 reference statements)

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“…These findings are consistent with findings of a previous study showing that glutamatergic cells in the MSDB remain tuned to running speed in the absence of optic flow (Justus et al, 2016) . The finding that visual inputs do not alter the temporal dynamics of cholinergic activity as a function of running speed are similar to findings in previous studies of a potential speed code by firing rate in neurons of the entorhinal cortex (Dannenberg et al, 2020) and posterior parietal cortex (Alexander et al, 2022) that demonstrated no change in the speed tuning of normalized firing rates. However, those studies showed a change in the gain of speed tuning of absolute firing rates.…”

Section: Discussionsupporting

confidence: 89%

“…Theoretical work has been shown that information from optical flow could contribute to coding of location and running speed in the medial entorhinal cortex (Raudies et al, 2012(Raudies et al, , 2016. Experimental data showing the contribution of visual inputs on the spatial accuracy of grid cell firing in the medial entorhinal cortex (Chen et al, 2016;Pérez-Escobar et al, 2016;Dannenberg et al, 2020) support the idea that movement information from optical flow can contribute to speed coding in the hippocampal formation. We therefore tested the hypothesis that the relationship between the activity of cholinergic neurons in the MSDB and the animal's running speed is changed in the absence of visual information by testing the effect of darkness on the speed tuning of cholinergic activity using a linear mixed effects model of data obtained from recordings under standard lighting conditions and darkness.…”

Section: The Activity Of Cholinergic Neurons Is Linearly Correlated W...mentioning

confidence: 88%

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Temporal dynamics of cholinergic activity in the septo-hippocampal system

Kopsick

Hartzell

Lazaro

et al. 2022

Preprint

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Cholinergic projection neurons in the medial septum and diagonal band of Broca are the major source of cholinergic modulation of hippocampal circuit functions that support neural coding of location and running speed. Changes in cholinergic modulation are known to correlate with changes in brain states, cognitive functions, and behavior. However, whether cholinergic modulation can change fast enough to serve as a potential speed signal in hippocampal and parahippocampal cortices and whether the temporal dynamics in such a signal depend on the presence of visual cues remain unknown. In this study, we use a fiber-photometric approach to quantify the temporal dynamics of cholinergic activity in freely moving mice as a function of the animal's running speed and visual cues. We show that the population activity of cholinergic neurons in the medial septum and diagonal band of Broca changes fast enough to be aligned well with changes in the animal's running speed and is strongly and linearly correlated to the logarithm of the animal's running speed. Intriguingly, the cholinergic modulation remains strongly and linearly correlated to the speed of the animal's neck movements during periods of stationary activity. Furthermore, we show that cholinergic modulation is unaltered during darkness. Lastly, we identify rearing, a discrete behavior where the mouse stands on its hindlimbs to scan the environment from an elevated perspective, is associated with higher cholinergic activity than expected from neck movements on the horizontal plane alone. Taken together, these data show that temporal dynamics in the cholinergic modulation of hippocampal circuits are fast enough to provide a potential running speed signal in real-time. Moreover, the data show that cholinergic modulation is primarily a function of the logarithm of the animal's movement speed, both during locomotion and during stationary activity, with no significant interaction with visual inputs. These data advance our understanding of temporal dynamics in cholinergic modulation of hippocampal circuits and their functions in the context of neural coding of location and running speed.

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Section: Discussionsupporting

confidence: 89%

Section: The Activity Of Cholinergic Neurons Is Linearly Correlated W...mentioning

confidence: 88%

Temporal dynamics of cholinergic activity in the septo-hippocampal system

Kopsick

Hartzell

Lazaro

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…The precise mechanisms of how speed and HD information are combined remain unclear, but several studies have suggested that speed cells may be more closely linked to grid cell firing than HD cells ( 189 , 193 , 209 ). Similar to grid and HD cells, the firing of speed cells is mostly context independent ( 135 ), although some changes in the speed code have been reported, for instance in darkness ( 62 , 150 , 210 ), when the shape or size of the environment is changed ( 189 ), or even when a visual pattern is changed along a linear track ( 62 ). The finding that changes in speed cell firing tend to be correlated with changes in grid cell coding suggests that speed cells may be embedded in functional grid cell modules, possibly providing part of the velocity input needed to shift activity bumps in CAN models.…”

Section: Functionally Defined Cell Typesmentioning

confidence: 99%

Microcircuits for spatial coding in the medial entorhinal cortex

Tukker

Beed

Brecht

et al. 2022

Physiological Reviews

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The hippocampal formation is critically involved in learning and memory, and contains a large proportion of neurons encoding aspects of the organism's spatial surroundings. In the medial entorhinal cortex (MEC), this includes grid cells with their distinctive hexagonal firing fields, as well as a host of other functionally defined cell types including head-direction cells, speed cells, border cells, and object vector cells. Such spatial coding emerges from the processing of external inputs by local microcircuits. However, it remains unclear exactly how local microcircuits and their dynamics within the MEC contribute to spatial discharge patterns. In this review we focus on recent investigations of intrinsic MEC connectivity, which have started to describe and quantify both excitatory and inhibitory wiring in the superficial layers of the MEC. Although the picture is far from complete, it appears that these layers contain robust recurrent connectivity that could sustain the attractor dynamics posited to underlie grid-pattern formation. These findings pave the way to a deeper understanding of the mechanisms underlying spatial navigation and memory.

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“…For example, horizontally displacing a visual cue in an environment reliably causes a concomitant shift in the preferred firing direction (PFD) of HD cells 21 . However, many studies have reported that HD cell responses are relatively stable in the absence of visual inputs or visual cues 14 , 26 – 28 . Furthermore, recordings from HD cells in young rodents just before eye-opening revealed tuned HD cells, although tuning curves were found to be broader than following eye-opening 22 , 29 , 30 .…”

Section: Introductionmentioning

confidence: 99%

Flexible cue anchoring strategies enable stable head direction coding in both sighted and blind animals

2022

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Vision plays a crucial role in instructing the brain’s spatial navigation systems. However, little is known about how vision loss affects the neuronal encoding of spatial information. Here, recording from head direction (HD) cells in the anterior dorsal nucleus of the thalamus in mice, we find stable and robust HD tuning in rd1 mice, a model of photoreceptor degeneration, that go blind by approximately one month of age. In contrast, placing sighted animals in darkness significantly impairs HD cell tuning. We find that blind mice use olfactory cues to maintain stable HD tuning and that prior visual experience leads to refined HD cell tuning in blind rd1 adult mice compared to congenitally blind animals. Finally, in the absence of both visual and olfactory cues, the HD attractor network remains intact but the preferred firing direction of HD cells drifts over time. These findings demonstrate flexibility in how the brain uses diverse sensory information to generate a stable directional representation of space.

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Effects of visual inputs on neural dynamics for coding of location and running speed in medial entorhinal cortex

Cited by 30 publications

References 89 publications

Temporal dynamics of cholinergic activity in the septo-hippocampal system

Temporal dynamics of cholinergic activity in the septo-hippocampal system

Microcircuits for spatial coding in the medial entorhinal cortex

Flexible cue anchoring strategies enable stable head direction coding in both sighted and blind animals

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