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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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Spatial stability of model grid cell responses before, during, and after MS inactivation (Case 2). Same as green plots in panels (C) and (F) of Figure 4, but with the stability of spatial responses computed in four different ways. Panels (A) and (B) correspond to the two entorhinal SOMs, respectively. In particular, for a given map cell that has a gridness score > 0 in the baseline trial (i.e., the one before MS is inactivated), the linear correlations between its baseline rate map and its rate maps from pertinent trials are calculated with the consideration of only those spatial bins with a non-zero rate in at least one trial (blue, triangle: Langston et al., 2010; Wills et al., 2010); only those bins with a non-zero rate in both trials (green, square); all bins without any restriction (red, hexagon: Koenig et al., 2011); and only those bins with a non-zero occupancy in both trials (cyan, circle: Brandon et al., 2011).
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Figure 7: Spatial stability of model grid cell responses before, during, and after MS inactivation (Case 2). Same as green plots in panels (C) and (F) of Figure 4, but with the stability of spatial responses computed in four different ways. Panels (A) and (B) correspond to the two entorhinal SOMs, respectively. In particular, for a given map cell that has a gridness score > 0 in the baseline trial (i.e., the one before MS is inactivated), the linear correlations between its baseline rate map and its rate maps from pertinent trials are calculated with the consideration of only those spatial bins with a non-zero rate in at least one trial (blue, triangle: Langston et al., 2010; Wills et al., 2010); only those bins with a non-zero rate in both trials (green, square); all bins without any restriction (red, hexagon: Koenig et al., 2011); and only those bins with a non-zero occupancy in both trials (cyan, circle: Brandon et al., 2011).

Mentions: The lower spatial stability of model grid cells in the trial coinciding with MS inactivation, compared to the immediately prior one, was ascertained in several ways. Figure 7 confirms this result for four different criteria to include positions, or bins, across the environment in the computation of inter-trial linear correlations of spatial rate maps; namely, regarding (a) only those bins where the firing rate is greater than zero in either trial (Langston et al., 2010; Wills et al., 2010), (b) only those bins where the firing rate is greater than zero in both trials, (c) all bins without any condition (Koenig et al., 2011), and (d) only those bins that were visited by the model animal in both trials (Brandon et al., 2011). To further establish that the decrease in spatial stability is not just due to missing grid firing fields, the model animal was made to run in two trials along the same realistic trajectory and with no further online changes in the strengths of connections from stripe cells to entorhinal map cells. In addition, the second trial involved reductions in cell response rates to one-fourth of their normal values. This allowed for the focused comparisons of spatial and temporal responses of model grid cells between the active and inactive MS conditions. Figure 8 provides observations of two representative model grid cells, one from each of the two entorhinal populations. For either cell, the rectified subtraction of the spatial rate map corresponding to the former trial from that of the latter trial reveals various inconsistent, or non-preferred, positions where the cell became active owing to MS inactivation. This is also clearly apparent in the membrane potential dynamics of the cells between the two trials, with reduced overlap between above-threshold activities.


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)

Spatial stability of model grid cell responses before, during, and after MS inactivation (Case 2). Same as green plots in panels (C) and (F) of Figure 4, but with the stability of spatial responses computed in four different ways. Panels (A) and (B) correspond to the two entorhinal SOMs, respectively. In particular, for a given map cell that has a gridness score > 0 in the baseline trial (i.e., the one before MS is inactivated), the linear correlations between its baseline rate map and its rate maps from pertinent trials are calculated with the consideration of only those spatial bins with a non-zero rate in at least one trial (blue, triangle: Langston et al., 2010; Wills et al., 2010); only those bins with a non-zero rate in both trials (green, square); all bins without any restriction (red, hexagon: Koenig et al., 2011); and only those bins with a non-zero occupancy in both trials (cyan, circle: Brandon et al., 2011).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Spatial stability of model grid cell responses before, during, and after MS inactivation (Case 2). Same as green plots in panels (C) and (F) of Figure 4, but with the stability of spatial responses computed in four different ways. Panels (A) and (B) correspond to the two entorhinal SOMs, respectively. In particular, for a given map cell that has a gridness score > 0 in the baseline trial (i.e., the one before MS is inactivated), the linear correlations between its baseline rate map and its rate maps from pertinent trials are calculated with the consideration of only those spatial bins with a non-zero rate in at least one trial (blue, triangle: Langston et al., 2010; Wills et al., 2010); only those bins with a non-zero rate in both trials (green, square); all bins without any restriction (red, hexagon: Koenig et al., 2011); and only those bins with a non-zero occupancy in both trials (cyan, circle: Brandon et al., 2011).
Mentions: The lower spatial stability of model grid cells in the trial coinciding with MS inactivation, compared to the immediately prior one, was ascertained in several ways. Figure 7 confirms this result for four different criteria to include positions, or bins, across the environment in the computation of inter-trial linear correlations of spatial rate maps; namely, regarding (a) only those bins where the firing rate is greater than zero in either trial (Langston et al., 2010; Wills et al., 2010), (b) only those bins where the firing rate is greater than zero in both trials, (c) all bins without any condition (Koenig et al., 2011), and (d) only those bins that were visited by the model animal in both trials (Brandon et al., 2011). To further establish that the decrease in spatial stability is not just due to missing grid firing fields, the model animal was made to run in two trials along the same realistic trajectory and with no further online changes in the strengths of connections from stripe cells to entorhinal map cells. In addition, the second trial involved reductions in cell response rates to one-fourth of their normal values. This allowed for the focused comparisons of spatial and temporal responses of model grid cells between the active and inactive MS conditions. Figure 8 provides observations of two representative model grid cells, one from each of the two entorhinal populations. For either cell, the rectified subtraction of the spatial rate map corresponding to the former trial from that of the latter trial reveals various inconsistent, or non-preferred, positions where the cell became active owing to MS inactivation. This is also clearly apparent in the membrane potential dynamics of the cells between the two trials, with reduced overlap between above-threshold activities.

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