Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues

Abstract

The representation of an animal's position in the medial entorhinal cortex (MEC) is distributed across several modules of grid cells, each characterized by a distinct spatial scale. The population activity within each module is tightly coordinated and preserved across environments and behavioral states. Little is known, however, about the coordination of activity patterns across modules. We analyzed the joint activity patterns of hundreds of grid cells simultaneously recorded in animals that were foraging either in the light, when sensory cues could stabilize the representation, or in darkness, when such stabilization was disrupted. We found that the states of different grid modules are tightly coordinated, even in darkness, when the internal representation of position within the MEC deviates substantially from the true position of the animal. These findings suggest that internal brain mechanisms dynamically coordinate the representation of position in different modules, to ensure that grid cells jointly encode a coherent and smooth trajectory of the animal.

Task-anchored grid cell firing is selectively associated with successful path integration-dependent behaviour

“…Together, these data indicate that grid cells can switch between task-anchored and task-independent firing modes within a behavioural session. This switching happens coherently across grid cell populations, which is consistent with grid cells forming networks with continuous attractor dynamics (Barry et al, 2007; Gardner et al, 2021; Waaga et al, 2021; Yoon et al, 2013). Our data also suggest that non-grid cells within the MEC form multiple populations, with some having activity that is coherent with the grid cell network, whereas others do not show task-independent periodic firing but instead maintain stable spatial representations independently from grid cells.…”

“…Given that populations of grid cells show coordinated dynamics that are consistent with their forming networks with continuous attractor dynamics (Barry et al, 2007; Waaga et al, 2021, 2021; Yoon et al, 2013), changes in anchoring should be coherent across grid cells and any non-grid cells that coordinate with the grid network. To test this, we compared activity patterns of simultaneously recorded grid and non-grid cells (Figure 4).…”

“…Since task-anchored firing fields could be read out directly to estimate track location, but location may only be inferred indirectly from task-independent activity, we reasoned that the presence or absence of task-anchoring could be used to assess whether grid firing contributes to the ongoing behaviour. Because in grid networks the activity of an individual neuron is informative about the network state as a whole (Fiete et al, 2008; Gardner et al, 2021; Waaga et al, 2021), then in principle activity of any grid cell is indicative of whether the grid network as a whole is in a task-anchored or task-independent mode (See also Figure 4). Thus, if anchoring of grid representations to the task environment is critical for localisation of the reward, then task-anchored coding of individual neurons should predict successful trials.…”

Task-anchored grid cell firing is selectively associated with successful path integration-dependent behaviour

“…Given that populations of grid cells show coordinated dynamics that are consistent with their forming networks with continuous attractor dynamics ( Barry et al, 2007 ; Waaga et al, 2021 ; Yoon et al, 2013 ), changes in anchoring should be coherent across grid cells and any non-grid cells that coordinate with the grid network. To test this, we compared activity patterns of simultaneously recorded grid and non-grid cells ( Figure 4 ).…”

Five discoveries of Volodymyr Betz. Part one. Betz and the islands of entorhinal cortex

“…Currently, the mechanism of formation of the typical spatial-preferential grid cell activity is unidentified (Witter, Doan, et al, 2017;Naumann et al, 2018;Tukker et al, 2022), the evidence about contribution of the stellate and pyramidal neurons of the MEC layer II in the formation of the grid cell specific activity is fragmental (Naumann et al, 2018), and the mechanisms of interdependence of the various navigation system cell are shrouded in darkness (E.I. Moser et al, 2017;Rowland et al, 2018;Angelaki & Laurens, 2020;Tukker et al, 2022), and the role of visual and other types of information for the peculiar grid cell activity is the subject of hypotheses (Connor & Knierim, 2017;Campbell & Giocomo, 2018;Jacob, Capitano, Poucet, Save, & Sargolini, 2019;Jayakumar et al, 2019;Moon, Gauthier, Park, Faivre & Blanke, 2022;Waaga et al, 2022). Although, there exists a considerable number of models, aimed to answer this questions (Finkel- Naumann et al, 2018;Widloski, Marder & Fiete, 2018;Kang & Balasubramanian, 2019;Mosheiff & Burak, 2019;Park, Jang, Kim & Kwag, 2019;Rodríguez-Domínguez & Caplan, 2019;Spalla, Dubreuil, Rosay, Monasson, & Treves, 2019;Agmon & Burak, 2020;D'Albis & Kempter, 2020;Ekstrom, Harootonian & Huffman, 2020;Vinepinsky, Perchik, & Segev, 2020;Waniek, 2020;Krishna et al, 2021;Rueckemann, Sosa, Giocomo & Buffalo, 2021;T.…”