Neural encoding of large-scale three-dimensional space—properties and constraints

Abstract

How the brain represents represent large-scale, navigable space has been the topic of intensive investigation for several decades, resulting in the discovery that neurons in a complex network of cortical and subcortical brain regions co-operatively encode distance, direction, place, movement etc. using a variety of different sensory inputs. However, such studies have mainly been conducted in simple laboratory settings in which animals explore small, two-dimensional (i.e., flat) arenas. The real world, by contrast, is complex and three dimensional with hills, valleys, tunnels, branches, and—for species that can swim or fly—large volumetric spaces. Adding an additional dimension to space adds coding challenges, a primary reason for which is that several basic geometric properties are different in three dimensions. This article will explore the consequences of these challenges for the establishment of a functional three-dimensional metric map of space, one of which is that the brains of some species might have evolved to reduce the dimensionality of the representational space and thus sidestep some of these problems.

Are There Place Cells in the Avian Hippocampus?

“…As the bat flies, and the vector between the moving bat and its goal changes, different goal direction cells become active or fall silent [Sarel et al, 2017]. Rats spatial neurons, in contrast, appear to reduce the problem of navigating in 3D space to navigation in a 2D plane, even when that plane is inclined, vertical, or inverted [Jeffrey et al, 2015]. Rat spatial neurons treat the plane of locomotion as the space in which orientation occurs, sometimes with loss of resolution if the plane of locomotion departs from the horizontal.…”

Claustrum of the short‐tailed fruit bat,Carollia perspicillata: Alignment of cellular orientation and functional connectivity

“…The only other bat claustrum report focused on the interconnections of auditory cortex and showed connectivity of the latter with frontal, anterior cingulate, retrosplenial and perirhinal cortices, the claustrum, and subcortical targets including the amygdala, auditory thalamus, pons, pretectum, superior and inferior colliculi, and central gray (Fitzpatrick et al, ). As described in the introduction, place, head‐direction, and grid cell recordings during navigational behavior have shown that individual place cells in bats are active in confined 3D volumes and nearly all neurons encode all three axes with similar resolution (Yartsev and Ulanovsky, ), whereas cells in rodents are multiplanar, but not fully volumetric (Stackman et al, ; Hayman et al, , ; Taube and Shinder, ; Taube et al, ; Jeffery et al, ). We speculate that a major basis for the multiplanar cell streams of the bat claustrum compared with rodent is the need for bats to function in three dimensions, and make decisions based on multisensory input in flight at higher speed with little margin for error (see e.g., Bar et al, ; Marshall et al, ).…”

“…Bats have been shown to differ from rodents in the activity of specific brain regions and circuits. Studies of place, head‐direction, and grid cells in navigational behavior have shown clear coding of three dimensions in bats (Yartsev and Ulanovsky, ), but only variations of two‐dimensional coding in rodents (Stackman et al, ; Hayman et al, , ; Taube and Shinder, ; Taube et al, ; Jeffery et al, ). These findings demonstrate functional differences between theses species and reinforce the idea that the two‐dimensional existence of rodents and the three‐dimensional existence of bats are different.…”

The place-cell representation of volumetric space in rats

“…Place cells are neurons in the hippocampus that fire when an animal visits specific regions of its environment, called place fields, and are thought to provide the foundation for an internal representation of space, or ‘cognitive map’ 1, 2 . The question arises as to whether this map is three-dimensional, and if so whether its properties are the same in all dimensions, and how information is integrated across these dimensions 3–5 . This is important not just for spatial mapping per se but also because the spatial map may form the framework for other types of cognition in which information dimensionality is higher than in real space.…”