On the nature of three‐dimensional encoding in the cognitive map: Commentary on Hayman, Verriotis, Jovalekic, Fenton, and Jeffery

Abstract

A recent article by Hayman, Verriotis, Jovalekic, Fenton, and Jeffery titled Anisotropic encoding of three-dimensional space by place cells and grid cells (2011) explored how place and grid cells respond when rats locomote vertically above the ground. From their results the authors concluded a number of points about rats’ abilities to orient and navigate in three dimensions. Here, we review evidence revolving around several issues including: 1) what reference frame rats use when locomoting vertically, 2) whether rats can perceive their height above the ground, 3) whether rats can estimate vertical distance and have a cognitive map in the vertical domain, 4) whether rats can path integrate in the vertical domain, and 5) does processing 3-dimensional representations require a large number of neurons. We argue that the Hayman et al. results can be accounted for by considering the reference frame the animals used in the tasks. Had the rats been facing inward with their limbs in contact with the vertical surface when moving, it is possible that different patterns of place and grid cell activity would have been observed. Further, there is good evidence to indicate that rats can orient and navigate effectively in the vertical domain.

“Right Door,” wrong floor: A canine deficiency in navigation

“…The critical points raised by Taube and Shinder (2013) may also be valid for the neurophysiological interpretation of our findings on anisotropic navigation of dogs in multilevel buildings. Nevertheless, the observation of their weak performance in identifying the right floor when using a staircase is striking and requires further experiments in which the reference frames for horizontal and vertical planes provide equivalent cues.…”

“…The authors hypothesized that rat cognitive maps may be contextually modulated and twodimensional rather than volumetric and three-dimensional. However, Taube and Shinder (2013) argue that the results can be accounted for by considering the reference frame used by the animals in the task and present experimental evidence of the capability of rats for orienting and navigating in the vertical domain.…”

Resolving the active versus passive conundrum for head direction cells

“…The importance of referencing the vestibular sensory information externally (to gravity) as opposed to internally (to the head), may not be clearly evident when the animal is moving with their head upright. However, as the animal moves in three dimensions, the difference in how sensory information is referenced defines whether the animal is able to continuously maintain orientation with its environment (Taube and Shinder, 2013). This view, that the cerebellum uses gravity to realign vestibular canal and otolith input in order to extract movement in the horizontal and vertical planes, has not been tested.…”

Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

“…The tuning curve of these neurons allows us to measure how their activity is related to incoming, highly-processed signals. The most-explored neuron types are the head-direction cells with a one-dimensional tuning curve, and place cells and grid cells with two-dimensional tuning curves (although the three types of neurons are known now to encompass one more dimension, namely the vertical plane (Taube and Shinder, 2013)). The neuronal activity of head-direction cells is represented by a Gaussian curve of the firing rate versus the animal's heading direction over 360 degrees.…”