Place cell maps slowly develop via competitive learning and conjunctive coding in the dentate gyrus

Abstract

Place cells exhibit spatially selective firing fields that collectively map the continuum of positions in environments; how such activity pattern develops with experience is largely unknown. Here, we record putative granule cells (GCs) and mossy cells (MCs) from the dentate gyrus (DG) over 27 days as mice repetitively run through a sequence of objects fixed onto a treadmill belt. We observe a progressive transformation of GC spatial representations, from a sparse encoding of object locations and spatial patterns to increasingly more single, evenly dispersed place fields, while MCs show little transformation and preferentially encode object locations. A competitive learning model of the DG reproduces GC transformations via the progressive integration of landmark-vector cells and spatial inputs and requires MC-mediated feedforward inhibition to evenly distribute GC representations, suggesting that GCs slowly encode conjunctions of objects and spatial information via competitive learning, while MCs help homogenize GC spatial representations.

Flexible encoding of objects and space in single cells of the dentate gyrus

“…While most cells maintained a stable, spatial map of the environment, the activity of many DG place cells was affected by the addition or displacement of objects within the environment. Many cells resembled LV cells previously reported in the hippocampus (and similar object-vector cells in entorhinal cortex), 4, 17, 30 with multiple firing fields that shared the same vector relationship to multiple objects. Other cells had place fields that moved when a nearby object was moved, fields that appeared, disappeared, rotated, or moved closer to an object, as well as trace firing at previous object locations.…”

“…Recent studies have reported how tactile cues affect DG activity during learning in head-fixed mice. 30, 31 While mossy cells encoded cue locations throughout learning, cue-associated activity in granule cells was more common early in training. 31 The well-trained task used in the present study may therefore reduce the prevalence of object-related granule cell activity.…”

“…In head-fixed mice, the addition of tactile cues to a treadmill has been shown to induce or reorganize some granule cell and mossy cell firing fields and revealed differences between the cell types in the timing and duration of cue-modulated firing during learning. 30–32 Given the well-established ability of the hippocampus to generate highly stereotyped sequential representations of distance and time in linear tracks and treadmills, it can be difficult to disentangle neural responses to tactile cues and spatial information that is repeatedly experienced by the animal in a particular order. Therefore, it is also critical to record from freely-moving animals in a 2D environment to determine how spatial and non-spatial information is represented when not constrained by sequential presentations of stimuli and path-invariant sampling of space, which has been challenging due to technical difficulties in recording and identifying different DG cell types in vivo.…”

Flexible encoding of objects and space in single cells of the dentate gyrus

“…In head-fixed mice, the addition of tactile cues to a treadmill induced or reorganized some granule cell and mossy cell firing fields and revealed differences between the cell types in the timing and duration of cue-modulated firing during learning. [32][33][34] Given the well-established ability of the hippocampus to generate highly stereotyped sequential representations of distance and time in linear tracks and treadmills, it can be difficult to disentangle neural responses to spatial information and tactile cues that are repeatedly experienced by the animal in a particular order. Therefore, it is critical to record from freely moving animals in an environment in which objects can be approached from multiple directions in a 2D coordinate frame to determine how spatial and nonspatial information is represented when not constrained by sequential presentations of stimuli and path-invariant sampling of space.…”

Dentate granule cells encode auditory decisions after reinforcement learning in rats

“…Our findings suggest that DGCs form similar maps in the dentate gyrus after auditory task learning. We performed 5 days of habituation in the decision task apparatus to exclude the neural dynamics from learning the context, however, Kim et al 40 recently showed that the slow emergence of dentate spatial maps plateaus after a week. This could potentially explain the neural activity pattern in “off task” assemblies to RS II or III more than RS I.…”