The Preferred Directions of Conjunctive Grid X Head Direction Cells in the Medial Entorhinal Cortex Are Periodically Organized

Abstract

The discovery of speed-modulated grid, head direction, and conjunctive grid x head direction cells in the medial entorhinal cortex has led to the hypothesis that path integration, the updating of one’s spatial representation based on movement, may be carried out within this region. This hypothesis has been formalized by many computational models, including a class known as attractor network models. While many of these models propose specific mechanisms by which path integration might occur, predictions of these specific mechanisms have not been tested. Here I derive and test a key prediction of one attractor network path integration mechanism. Specifically, I first demonstrate that this mechanism predicts a periodic distribution of conjunctive cell preferred directions in order to minimize drift. Next, I test whether conjunctive cell preferred directions are in fact periodically organized. Results indicate that conjunctive cells are preferentially tuned to increments of 36°, consistent with drift minimization in this path integration mechanism. By contrast, no periodicity was observed in the preferred directions of either pure grid or pure head direction cells. These results provide the first neural evidence of a nonuniform structure in the directional preferences of any head direction representation found in the brain.

Mesoscopic Neural Representations in Spatial Navigation

“…The "conjunctive grid by head-direction cell hypothesis" (Fig. 3B) builds upon prior research which suggested that the firing of conjunctive grid by head-direction cells located in deeper layers of the EC and in pre-and parasubiculum [71] is aligned with the grid axes ( [14]; but see [111]). Assuming that the directional tuning width of these conjunctive grid by head-direction cells is not too broad, movements aligned with the grid axes (as compared to misaligned movements) will result in increased spiking activity of the conjunctive grid by head-direction cell population -thus causing the appearance of meso-/macroscopic grid-like representations [14].…”

Orientation Invariant Sensorimotor Object Recognition Using Cortical Grid Cells

“…Conjunctive cells are closely related to grid cells, incorporating multiple navigational signals such as direction and position for path integration mechanisms. Attractor networks are popular for modeling path integration with these cells, and have been shown to predict a periodic distribution of conjunctive cell preferred directions (Keinath, 2016 ). Keinath ( 2016 ) found that cells were tuned in periodic increments, with a lower bound of 10° and an upper bound of 120° between preferred directions.…”

“…Attractor networks are popular for modeling path integration with these cells, and have been shown to predict a periodic distribution of conjunctive cell preferred directions (Keinath, 2016 ). Keinath ( 2016 ) found that cells were tuned in periodic increments, with a lower bound of 10° and an upper bound of 120° between preferred directions. These results resonate with the aforementioned primary orientations of the proposed model, indicating that conjunctive cells could be a biological correlate for equivalently rotating an orientation reference (which produces such periodic distributions of preferred directions).…”

What are grid-like responses doing in the orbitofrontal cortex?

“…In humans, grid-like neural activity has been identified using two different methods: direct electrophysiological recordings using intracranial electroencephalography (iEEG) in epilepsy patients (Jacobs et al, 2013; Nadasdy et al, 2017); and functional magnetic resonance imaging (fMRI) methods that indirectly and non-invasively capture grid-like responses in healthy individuals (Bao et al, 2019; Bellmund et al, 2016; Constantinescu et al, 2016; Doeller et al, 2010; He & Brown, 2019; Horner et al, 2016; Jacobs et al, 2013; Julian et al, 2018; Kim & Maguire, 2019; Kunz et al, 2015; Nau et al, 2018; Stangl et al, 2018). While a detailed explanation of how grid cell firing gives rise to grid-like fMRI responses is beyond the scope of this article, the basic idea is that if grid cells share a common orientation across neighboring cells (Barry et al, 2007; Doeller et al, 2010; Stensola et al, 2012; but see Keinath, 2016) and show preferential firing for movement aligned (vs. misaligned) with the main axes of the grid (Doeller et al, 2010), then one should be able to detect their presence via measures of neural population activity, such as fMRI (Doeller et al, 2010; for review, see Kriegeskorte & Storrs, 2016; Figure 2). That is, neural population activity as measured using the blood oxygenation level-dependent (BOLD) signal should be relatively higher on trials in which movements occur in alignment with the six main axes of the grid…”