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How reduction of theta rhythm by medial septum inactivation may covary with disruption of entorhinal grid cell responses due to reduced cholinergic transmission.

Pilly PK, Grossberg S - Front Neural Circuits (2013)

Bottom Line: Two recent studies reduced the theta rhythm by inactivating the medial septum (MS) and demonstrated a correlated reduction in the characteristic hexagonal spatial firing patterns of grid cells.In particular, the adverse effects of MS inactivation on grid cells can be understood in terms of how the concomitant reduction in cholinergic inputs may increase the conductances of leak potassium (K(+)) and slow and medium after-hyperpolarization (sAHP and mAHP) channels.These results demonstrate how models of grid cell self-organization can provide new insights into the relationship between brain learning and oscillatory dynamics.

View Article: PubMed Central - PubMed

Affiliation: Center for Neural and Emergent Systems, Information and Systems Sciences Laboratory, HRL Laboratories Malibu, CA, USA.

ABSTRACT
Oscillations in the coordinated firing of brain neurons have been proposed to play important roles in perception, cognition, attention, learning, navigation, and sensory-motor control. The network theta rhythm has been associated with properties of spatial navigation, as has the firing of entorhinal grid cells and hippocampal place cells. Two recent studies reduced the theta rhythm by inactivating the medial septum (MS) and demonstrated a correlated reduction in the characteristic hexagonal spatial firing patterns of grid cells. These results, along with properties of intrinsic membrane potential oscillations (MPOs) in slice preparations of medial entorhinal cortex (MEC), have been interpreted to support oscillatory interference models of grid cell firing. The current article shows that an alternative self-organizing map (SOM) model of grid cells can explain these data about intrinsic and network oscillations without invoking oscillatory interference. In particular, the adverse effects of MS inactivation on grid cells can be understood in terms of how the concomitant reduction in cholinergic inputs may increase the conductances of leak potassium (K(+)) and slow and medium after-hyperpolarization (sAHP and mAHP) channels. This alternative model can also explain data that are problematic for oscillatory interference models, including how knockout of the HCN1 gene in mice, which flattens the dorsoventral gradient in MPO frequency and resonance frequency, does not affect the development of the grid cell dorsoventral gradient of spatial scales, and how hexagonal grid firing fields in bats can occur even in the absence of theta band modulation. These results demonstrate how models of grid cell self-organization can provide new insights into the relationship between brain learning and oscillatory dynamics.

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Data showing effects of medial septum (MS) inactivation on grid cells and network theta oscillations in medial entorhinal cortex (MEC). (A) Examples of disruption in the spatial expression of the hexagonal grid structure for two grid cells (Brandon et al., 2011). (B) Temporal reduction in the power and frequency of network theta oscillations (Koenig et al., 2011). (C) Temporary reduction in the gridness score, mean firing rate, and spatial stability of grid cells (Koenig et al., 2011). [Data reprinted with permission from Brandon et al. (2011) and Koenig et al. (2011)].
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Figure 1: Data showing effects of medial septum (MS) inactivation on grid cells and network theta oscillations in medial entorhinal cortex (MEC). (A) Examples of disruption in the spatial expression of the hexagonal grid structure for two grid cells (Brandon et al., 2011). (B) Temporal reduction in the power and frequency of network theta oscillations (Koenig et al., 2011). (C) Temporary reduction in the gridness score, mean firing rate, and spatial stability of grid cells (Koenig et al., 2011). [Data reprinted with permission from Brandon et al. (2011) and Koenig et al. (2011)].

Mentions: Recently, Brandon et al. (2011) and Koenig et al. (2011) studied the effects of temporarily inactivating MS using infusions of muscimol and lidocaine, respectively, in dorsal MEC. They found that MS inactivation causes reductions in the power and frequency of MEC network theta oscillations, as well as in the hexagonal gridness quality, spatial stability, and firing rate of grid cells (Figure 1). As the effects of the drugs wash out, the recovery of grid cell properties coincides with that of the theta rhythm. One prominent interpretation of these data has been that the theta rhythm is essential for grid cells to express their spatially periodic firing fields, and thereby that oscillatory interference is indeed at play. Other recent data challenge this view by showing in various ways that the spatial firing fields of grid cells do not depend upon an ongoing theta rhythm (e.g., Yartsev et al., 2011; Killian et al., 2012; Domnisoru et al., 2013; Schmidt-Heiber and Hausser, 2013).


How reduction of theta rhythm by medial septum inactivation may covary with disruption of entorhinal grid cell responses due to reduced cholinergic transmission.

Pilly PK, Grossberg S - Front Neural Circuits (2013)

Data showing effects of medial septum (MS) inactivation on grid cells and network theta oscillations in medial entorhinal cortex (MEC). (A) Examples of disruption in the spatial expression of the hexagonal grid structure for two grid cells (Brandon et al., 2011). (B) Temporal reduction in the power and frequency of network theta oscillations (Koenig et al., 2011). (C) Temporary reduction in the gridness score, mean firing rate, and spatial stability of grid cells (Koenig et al., 2011). [Data reprinted with permission from Brandon et al. (2011) and Koenig et al. (2011)].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814006&req=5

Figure 1: Data showing effects of medial septum (MS) inactivation on grid cells and network theta oscillations in medial entorhinal cortex (MEC). (A) Examples of disruption in the spatial expression of the hexagonal grid structure for two grid cells (Brandon et al., 2011). (B) Temporal reduction in the power and frequency of network theta oscillations (Koenig et al., 2011). (C) Temporary reduction in the gridness score, mean firing rate, and spatial stability of grid cells (Koenig et al., 2011). [Data reprinted with permission from Brandon et al. (2011) and Koenig et al. (2011)].
Mentions: Recently, Brandon et al. (2011) and Koenig et al. (2011) studied the effects of temporarily inactivating MS using infusions of muscimol and lidocaine, respectively, in dorsal MEC. They found that MS inactivation causes reductions in the power and frequency of MEC network theta oscillations, as well as in the hexagonal gridness quality, spatial stability, and firing rate of grid cells (Figure 1). As the effects of the drugs wash out, the recovery of grid cell properties coincides with that of the theta rhythm. One prominent interpretation of these data has been that the theta rhythm is essential for grid cells to express their spatially periodic firing fields, and thereby that oscillatory interference is indeed at play. Other recent data challenge this view by showing in various ways that the spatial firing fields of grid cells do not depend upon an ongoing theta rhythm (e.g., Yartsev et al., 2011; Killian et al., 2012; Domnisoru et al., 2013; Schmidt-Heiber and Hausser, 2013).

Bottom Line: Two recent studies reduced the theta rhythm by inactivating the medial septum (MS) and demonstrated a correlated reduction in the characteristic hexagonal spatial firing patterns of grid cells.In particular, the adverse effects of MS inactivation on grid cells can be understood in terms of how the concomitant reduction in cholinergic inputs may increase the conductances of leak potassium (K(+)) and slow and medium after-hyperpolarization (sAHP and mAHP) channels.These results demonstrate how models of grid cell self-organization can provide new insights into the relationship between brain learning and oscillatory dynamics.

View Article: PubMed Central - PubMed

Affiliation: Center for Neural and Emergent Systems, Information and Systems Sciences Laboratory, HRL Laboratories Malibu, CA, USA.

ABSTRACT
Oscillations in the coordinated firing of brain neurons have been proposed to play important roles in perception, cognition, attention, learning, navigation, and sensory-motor control. The network theta rhythm has been associated with properties of spatial navigation, as has the firing of entorhinal grid cells and hippocampal place cells. Two recent studies reduced the theta rhythm by inactivating the medial septum (MS) and demonstrated a correlated reduction in the characteristic hexagonal spatial firing patterns of grid cells. These results, along with properties of intrinsic membrane potential oscillations (MPOs) in slice preparations of medial entorhinal cortex (MEC), have been interpreted to support oscillatory interference models of grid cell firing. The current article shows that an alternative self-organizing map (SOM) model of grid cells can explain these data about intrinsic and network oscillations without invoking oscillatory interference. In particular, the adverse effects of MS inactivation on grid cells can be understood in terms of how the concomitant reduction in cholinergic inputs may increase the conductances of leak potassium (K(+)) and slow and medium after-hyperpolarization (sAHP and mAHP) channels. This alternative model can also explain data that are problematic for oscillatory interference models, including how knockout of the HCN1 gene in mice, which flattens the dorsoventral gradient in MPO frequency and resonance frequency, does not affect the development of the grid cell dorsoventral gradient of spatial scales, and how hexagonal grid firing fields in bats can occur even in the absence of theta band modulation. These results demonstrate how models of grid cell self-organization can provide new insights into the relationship between brain learning and oscillatory dynamics.

Show MeSH
Related in: MedlinePlus