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Interactions between rodent visual and spatial systems during navigation

Nature Reviews Neuroscience volume 24, pages 487–501 (2023)Cite this article

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Abstract

Many behaviours that are critical for animals to survive and thrive rely on spatial navigation. Spatial navigation, in turn, relies on internal representations about one’s spatial location, one’s orientation or heading direction and the distance to objects in the environment. Although the importance of vision in guiding such internal representations has long been recognized, emerging evidence suggests that spatial signals can also modulate neural responses in the central visual pathway. Here, we review the bidirectional influences between visual and navigational signals in the rodent brain. Specifically, we discuss reciprocal interactions between vision and the internal representations of spatial position, explore the effects of vision on representations of an animal’s heading direction and vice versa, and examine how the visual and navigational systems work together to assess the relative distances of objects and other features. Throughout, we consider how technological advances and novel ethological paradigms that probe rodent visuo-spatial behaviours allow us to advance our understanding of how brain areas of the central visual pathway and the spatial systems interact and enable complex behaviours.

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Fig. 1: Brain areas that represent information related to space, vision and head direction.
Fig. 2: Visual control of spatial representations and spatial signals in visual areas.
Fig. 3: Influence of vision on head-direction cells and influences of head orientation on visual cortex activity.
Fig. 4: The influence of visual depth signals on visuo-spatial processing.

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Acknowledgements

The authors thank K. J. Jeffery and M. Huebener for feedback on an earlier version of the manuscript. This work was supported by Deutsche Forschungsgemeinschaft (DFG) SFB 1233 Robust Vision: Inference Principles and Neural Mechanisms TP 10/13 (project number: 276693517), DFG SFB 870 TP 19 (project number: 118803580), DFG BU 1808/6-2 and 1808/5-2, and a ONE Munich Strategy Forum grant (LMU Munich, TU Munich and the Bavarian Ministry for Science and Art) to L.B. This work was also supported by The Sir Henry Dale Fellowship from the Wellcome Trust and Royal Society (200501) and the Human Frontier in Science Program (RGY0076/2018) to A.B.S.

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Authors and Affiliations

  1. UCL Institute of Behavioural Neuroscience, Department of Experimental Psychology, University College London, London, UK

    Aman B. Saleem

  2. Division of Neuroscience, Faculty of Biology, LMU Munich, Munich, Germany

    Laura Busse

  3. Bernstein Centre for Computational Neuroscience Munich, Munich, Germany

    Laura Busse

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  1. Aman B. Saleem
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Glossary

Active sampling

A cognitive or behavioural strategy, in which an organism seeks out and acquires specific sensory information from its environment in an active process, as opposed to passively receiving sensory input.

Allocentric position

In a world-centric reference frame, defined with respect to external cues or landmarks and independent of the observer’s own position or orientation.

Corollary discharge

Often referred to as a neural signal that is obtained by passing a motor efference copy through a forward model of motor control. As the corollary discharge is then in sensory coordinates, it can be directly compared with sensory signals.

Distal cues

Cues that are large, stationary and so far away from the animal that they have fixed directional positions from anywhere within the environment. Distal cues are typically visual landmarks. Laboratory studies commonly refer to visual cues as distal if they are placed on the walls of the experimental room in which the arena is situated.

Efference copies

Copies of the motor commands sent from the motor areas of the brain to other regions, including sensory areas. This information can be used to predict (or generate an expectation for) the outcomes of the motor command.

Egocentric

In an observer-centric reference frame, defined relative to the observer’s features (for example, body position and orientation or eye position).

Gain fields

In the context of spatial representations, neural representations in which the activity of the neurons encodes both the location of a stimulus in the sensory space and the current state of the animal’s body. The firing rate is multiplicatively modulated by the position of the sensor (such as the eye or arm) or the animal and/or its orientation in space. This spatial tuning facilitates the integration of sensory information with body-centred information.

Gaze

The line of sight (per eye), determined by both the position of the eye in orbit (eye position) and the position of the head in space.

Grid cells

A type of neurons that display spatial selectivity, characterized by multiple firing fields arranged in a hexagonal grid pattern across the environment. These cells increase the firing rate when the animal moves through any of their fields and are thought to have a role in coding distances as the animal navigates its surroundings.

Head direction

The direction towards which the head of an animal is pointing.

Head-direction cells

(HD cells). Cells that exhibit their highest level of activity when the animal’s head is oriented towards a specific direction, remaining inactive in other directions. Different HD cells can be active in different directions, and when considered as a population, these cells collectively represent all possible directions.

Heading direction

The direction towards which the whole body of an animal is moving.

Landmarks

Distinctive features or objects in the environment that are stably related to specific locations or bearings on the map, and thus can be used as reference points for navigation.

Motion parallax

The perceptual phenomenon in which objects located at different distances from an observer appear to move at different speeds or directions when the observer moves. This serves as a monocular depth cue providing information about the relative distances between objects in the visual scene.

Object/boundary vector cells

A type of neurons that become active when an animal is located at a specific vectorial distance relative to an object or boundary in the environment.

Path integration

A navigational strategy used by animals to maintain an estimate of their current position in space. It consists of the accumulation of self-motion-related interoceptive information over time from an egocentric reference point.

Place cells

A type of neurons that exhibit heightened activity when an animal occupies a specific location in its environment (or a few positions in large environments), irrespective of the animal’s head direction.

Proximal cues

Cues that are small and often located within the animal’s immediate environment or very close to it, so that they can change their relative directional position as the animal moves around.

Reafferent visual input

The sensory information that is received by the visual system as a result of the interaction between an organism’s own movements and the external environment; that is, sensory signals generated by the movement of the eyes, head or body.

Saccadic suppression

A phenomenon in visual perception in which visual information is suppressed or reduced during saccadic movements. This is thought to prevent motion blur from reaching awareness and to support our uninterrupted visual experience.

Stereopsis

The perception of visual depth that arises from binocular disparity; that is, the slight difference in the visual input received by each eye due to their slightly different positions on the head.

Virtual reality

(VR). An artificial, simulated environment that updates in a manner that is contingent on one’s action. Human VR systems often use computer peripherals to capture a subject’s actions. Rodent VR systems instead typically use optical sensors or rotary encoders to capture a subject’s actions on a treadmill.

Visual depth

The distance or three-dimensional spatial relationships between objects (or other environmental features) estimated based on visual features in the scene.

VR gain

This is the relationship between the physical distance travelled by a subject on a treadmill (or other sensor) and the virtual distance travelled in a given virtual reality (VR) environment. Increasing gain refers to making larger movements in VR (and decreasing gain to smaller movements in VR) for the same physical distance travelled.

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Saleem, A.B., Busse, L. Interactions between rodent visual and spatial systems during navigation. Nat. Rev. Neurosci. 24, 487–501 (2023). https://doi.org/10.1038/s41583-023-00716-7

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