Study identifies a new building block in the navigation system of fish

Defining the basic inventory of spatial and kinematical cells in the goldfish telencephalon.

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The ability to navigate is among the essential cognitive abilities for the survival of fish, the most significant class of vertebrates, and nearly all other animal classes. The neurological foundation of navigation is significantly influenced by space encoding in single neurons.

The environment fish navigate through is one key distinction between fish and other vertebrates. Aquatic areas present a special set of navigational challenges. Unlike terrestrial animals, which are constrained by the world’s vertical dimension, fish may navigate in three dimensions.

A recent study tracked the activity of neurons in the central region of the goldfish telencephalon as the fish freely navigated in a quasi-2D water tank encased in a 3D environment to examine this essential cognitive component in fish. The goldfish were allowed to freely move about a water tank along its vertical and horizontal axes while the recordings were being made.

Before the recordings, researchers fed the fish in various locations within a rectangular water tank to train them to swim continually. The fish usually became accustomed to the water tank after 1–2 weeks of training sessions and adapted to freely exploring its surroundings. Scientists placed extracellular tetrodes and a wireless recording equipment in its central nervous system during the most recent training session.

The goldfish began exploring the quasi-2D water tank after spending a day recovering from the implant operation. Three to four tetrodes were used to record neural activity, and spike sorting was used to identify individual cells. This enabled researchers to examine links between fish trajectory and cell activity.

The findings demonstrated that the fish‘s position in its environment significantly influenced a substantial fraction of the recorded cells’ brain activity. They checked for insession stability, spatial coherence, and spatial information, as well as for crossing a spatial information threshold, to statistically test if this neuron encoded components of the position.

The similarity between the firing rate maps for the session’s first and second halves indicated in-session stability. The cell’s spatial coherence and spatial information were higher than the corresponding values for 5,000 shuffled spike trains generated using an interspike interval (ISI) shuffling procedure.

Not all boundary vector cells were tuned to boundaries in the vertical or horizontal directions. Instead, some cells had a firing pattern that gradually decreased with the distance of the fish from the corners of the water tank.

The study also investigated if the fish’s allocentric swimming direction affects the border vector cells’ activity. They display a heatmap of the firing rate to position for each cell, divided into the times when the fish was swimming in one of two directions: either towards or away from its preferred boundary direction.

It is still challenging to firmly distinguish the effect of allocentric swimming direction from other behavioral features in space, even if this data supports the idea that there is a directionality tuning in the activity of the border vector cells in fish. Therefore, additional research is required to prove this claim.

The presence of low-beta neuronal oscillations was another variation seen in fish. Numerous boundary-vector cells exhibited these oscillations in their activity, while researchers saw no oscillations in cells whose activity was not influenced by position. As far as we are aware, there have never been any reports of a relationship between spatial localization and beta oscillations.

It’s common knowledge that neural oscillations connected to spatial memory occur in the theta frequency band. The originality of spatial encoding in fish and the significance of rhythmic oscillations for spatial encoding is thus supported by these findings, which may represent a crucial component of the comparative approach to researching spatial encoding across species.

The findings presented here contribute to defining the basic inventory of spatial and kinematical cells in the goldfish telencephalon. The abundance of spatially modulated cells in the telencephalon’s central part underscores this brain region’s importance for navigation.

Scientists noted, “We found spatially modulated neurons with firing patterns that gradually decreased with the distance of the fish from a boundary in each cell’s preferred direction, resembling the boundary vector cells found in the mammalian subiculum. Many of these cells exhibited beta rhythm oscillations. This type of spatial representation in fish brains is unique among space-encoding cells in vertebrates and provides insights into spatial cognition in this lineage.”

Journal Reference:

  1. Cohen L, Vinepinsky E, Donchin O, Segev R (2023) Boundary vector cells in the goldfish central telencephalon encode spatial information. PLoS Biol 21(4): e3001747. DOI: 10.1371/journal.pbio.3001747